Publications by year
In Press
Boots M, wilfert, Bartlett L (In Press). A genotypic trade-off between constitutive resistance to viral infection and host growth rate. Evolution
Manley R, Boots M, Bayer-Wilfert L (In Press). Condition-dependent virulence of Slow Bee Paralysis Virus in Bombus terrestris: Are the impacts of honeybee viruses in wild pollinators underestimated?. Oecologia
Silk M, Weber NL, Steward LC, Hodgson D, Boots M, Croft DP, Delahay RJ, McDonald R (In Press). Contact networks structured by sex underpin sex-specific epidemiology of infection. Ecology Letters
Boots M, Bartlett L (In Press). Industrial bees: the impact of apicultural intensification on local disease 1 prevalence. Journal of Applied Ecology
Silk MJ, Hodgson D, Rozins C, Croft D, Delahay R, Boots M, McDonald R (In Press). Integrating social behaviour, demography and disease dynamics in network models: applications to disease management in declining wildlife populations. Philosophical Transactions B: Biological Sciences
Boots M, taggart S, tidbury H, bridgett S, garbutt J, kaur G (In Press). Novel insights into the insect transcriptome response to a natural DNA virus. BMC Genomics
Silk MJ, Drewe JA, Delahay RJ, Weber N, Steward LC, Wilson-Aggarwal J, Boots M, Hodgson DJ, Croft DP, McDonald RA, et al (In Press). Quantifying direct and indirect contacts for the potential transmission of infection between species using a multilayer contact network. Behaviour
Silk MJ, Webber N, Steward LC, Delahay RJ, Croft DP, Hodgson, Hodgson DJ, Boots M, McDonald RA (In Press). Seasonal variation in daily patterns of social contacts in the European badger Meles meles. Ecology and Evolution
Silk MJ, Croft DP, Delahay RJ, Hodgson DJ, Boots M, Weber N, McDonald RA (In Press). Using social network metrics in wildlife disease ecology, epidemiology and management. Bioscience
2023
Saad-Roy CM, Levin SA, Grenfell BT, Boots M (2023). Epidemiological impacts of post-infection mortality.
Proc Biol Sci,
290(2002).
Abstract:
Epidemiological impacts of post-infection mortality.
Infectious diseases may cause some long-term damage to their host, leading to elevated mortality even after recovery. Mortality due to complications from so-called 'long COVID' is a stark illustration of this potential, but the impacts of such post-infection mortality (PIM) on epidemic dynamics are not known. Using an epidemiological model that incorporates PIM, we examine the importance of this effect. We find that in contrast to mortality during infection, PIM can induce epidemic cycling. The effect is due to interference between elevated mortality and reinfection through the previously infected susceptible pool. In particular, robust immunity (via decreased susceptibility to reinfection) reduces the likelihood of cycling; on the other hand, disease-induced mortality can interact with weak PIM to generate periodicity. In the absence of PIM, we prove that the unique endemic equilibrium is stable and therefore our key result is that PIM is an overlooked phenomenon that is likely to be destabilizing. Overall, given potentially widespread effects, our findings highlight the importance of characterizing heterogeneity in susceptibility (via both PIM and robustness of host immunity) for accurate epidemiological predictions. In particular, for diseases without robust immunity, such as SARS-CoV-2, PIM may underlie complex epidemiological dynamics especially in the context of seasonal forcing.
Abstract.
Author URL.
Lion S, Sasaki A, Boots M (2023). Extending eco-evolutionary theory with oligomorphic dynamics.
Ecol Lett,
26 Suppl 1, S22-S46.
Abstract:
Extending eco-evolutionary theory with oligomorphic dynamics.
Understanding the interplay between ecological processes and the evolutionary dynamics of quantitative traits in natural systems remains a major challenge. Two main theoretical frameworks are used to address this question, adaptive dynamics and quantitative genetics, both of which have strengths and limitations and are often used by distinct research communities to address different questions. In order to make progress, new theoretical developments are needed that integrate these approaches and strengthen the link to empirical data. Here, we discuss a novel theoretical framework that bridges the gap between quantitative genetics and adaptive dynamics approaches. 'Oligomorphic dynamics' can be used to analyse eco-evolutionary dynamics across different time scales and extends quantitative genetics theory to account for multimodal trait distributions, the dynamical nature of genetic variance, the potential for disruptive selection due to ecological feedbacks, and the non-normal or skewed trait distributions encountered in nature. Oligomorphic dynamics explicitly takes into account the effect of environmental feedback, such as frequency- and density-dependent selection, on the dynamics of multi-modal trait distributions and we argue it has the potential to facilitate a much tighter integration between eco-evolutionary theory and empirical data.
Abstract.
Author URL.
Uricchio LH, Bruns EL, Hood ME, Boots M, Antonovics J (2023). Multimodal pathogen transmission as a limiting factor in host distribution.
Ecology,
104(3).
Abstract:
Multimodal pathogen transmission as a limiting factor in host distribution.
Theoretical models suggest that infectious diseases could play a substantial role in determining the spatial extent of host species, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency-dependent transmission could have especially strong effects on the limits of species' distributions because diseased hosts that are sterilized but not killed may continue to produce infectious stages and frequency-dependent transmission mechanisms are effective even at very low population densities. We collected spatial pathogen prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogen Microbotryum dianthorum, a parasite that is spread through both frequency-dependent (vector-borne) and density-dependent (aerial spore transmission) mechanisms. Our 13-year study reveals rapid declines in population abundance without a compensatory decrease in pathogen prevalence. We apply a stochastic, spatial model of parasite spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency-dependent and density-dependent) transmission. We found that the observed rate of population decline could plausibly be explained by multimodal transmission, but is unlikely to be explained by either frequency-dependent or density-dependent mechanisms alone. Multimodal pathogen transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature.
Abstract.
Author URL.
Brook CE, Rozins C, Guth S, Boots M (2023). Reservoir host immunology and life history shape virulence evolution in zoonotic viruses.
PLoS Biology,
21(9).
Abstract:
Reservoir host immunology and life history shape virulence evolution in zoonotic viruses
The management of future pandemic risk requires a better understanding of the mechanisms that determine the virulence of emerging zoonotic viruses. Meta-analyses suggest that the virulence of emerging zoonoses is correlated with but not completely predictable from reservoir host phylogeny, indicating that specific characteristics of reservoir host immunology and life history may drive the evolution of viral traits responsible for cross-species virulence. In particular, bats host viruses that cause higher case fatality rates upon spillover to humans than those derived from any other mammal, a phenomenon that cannot be explained by phylogenetic distance alone. In order to disentangle the fundamental drivers of these patterns, we develop a nested modeling framework that highlights mechanisms that underpin the evolution of viral traits in reservoir hosts that cause virulence following cross-species emergence. We apply this framework to generate virulence predictions for viral zoonoses derived from diverse mammalian reservoirs, recapturing trends in virus-induced human mortality rates reported in the literature. Notably, our work offers a mechanistic hypothesis to explain the extreme virulence of bat-borne zoonoses and, more generally, demonstrates how key differences in reservoir host longevity, viral tolerance, and constitutive immunity impact the evolution of viral traits that cause virulence following spillover to humans. Our theoretical framework offers a series of testable questions and predictions designed to stimulate future work comparing cross-species virulence evolution in zoonotic viruses derived from diverse mammalian hosts.
Abstract.
Visher E, Ali A, Barajas J, Masud S, McBride A, Ramos E, Sui M, Villalobos-Heredia C, Walzer N, White PS, et al (2023). The direction of local adaptation on pathogen exploitation rates reverses with environmental context.
O'Neill X, White A, Boots M (2023). The evolution of parasite virulence under targeted culling and harvesting in wildlife and livestock.
EVOLUTIONARY APPLICATIONS Author URL.
2022
Sasaki A, Lion S, Boots M (2022). Antigenic escape selects for the evolution of higher pathogen transmission and virulence.
NATURE ECOLOGY & EVOLUTION,
6(1), 51-+.
Author URL.
Guth S, Mollentze N, Renault K, Streicker DG, Visher E, Boots M, Brook CE (2022). Bats host the most virulent-but not the most dangerous-zoonotic viruses.
Proc Natl Acad Sci U S A,
119(14).
Abstract:
Bats host the most virulent-but not the most dangerous-zoonotic viruses.
SignificanceThe clear need to mitigate zoonotic risk has fueled increased viral discovery in specific reservoir host taxa. We show that a combination of viral and reservoir traits can predict zoonotic virus virulence and transmissibility in humans, supporting the hypothesis that bats harbor exceptionally virulent zoonoses. However, pandemic prevention requires thinking beyond zoonotic capacity, virulence, and transmissibility to consider collective "burden" on human health. For this, viral discovery targeting specific reservoirs may be inefficient as death burden correlates with viral, not reservoir, traits, and depends on context-specific epidemiological dynamics across and beyond the human-animal interface. These findings suggest that longitudinal studies of viral dynamics in reservoir and spillover host populations may offer the most effective strategy for mitigating zoonotic risk.
Abstract.
Author URL.
Brook CE, Rozins C, Bohl JA, Ahyong V, Chea S, Fahsbender L, Huy R, Lay S, Leang R, Li Y, et al (2022). Climate, demography, immunology, and virology combine to drive two decades of dengue virus dynamics in Cambodia.
Lion S, Sasaki A, Boots M (2022). Extending eco-evolutionary theory with oligomorphic dynamics.
Uricchio LH, Bruns EL, Hood M, Boots M, Antonovics J (2022). Multimodal disease transmission as a limiting factor for the spatial extent of a host plant.
Lion S, Boots M, Sasaki A (2022). Multimorph Eco-Evolutionary Dynamics in Structured Populations. The American Naturalist, 200(3), 345-372.
Hockerstedt L, Numminen E, Ashby B, Boots M, Norberg A, Laine A-L (2022). Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease.
NATURE COMMUNICATIONS,
13(1).
Author URL.
Visher E, Mahjoub H, Soufi K, Pascual N, Hoang V, Bartlett LJ, Roberts K, Meaden S, Boots M (2022). The evolution of host resistance to a virus is determined by resources, historical contingency, and time scale.
Visher E, Uricchio L, Bartlett L, DeNamur N, Yarcan A, Alhassani D, Boots M (2022). The evolution of host specialization in an insect pathogen.
Evolution,
76(10), 2375-2388.
Abstract:
The evolution of host specialization in an insect pathogen.
Niche breadth coevolution between biotic partners underpins theories of diversity and co-existence and influences patterns of disease emergence and transmission in host-parasite systems. Despite these broad implications, we still do not fully understand how the breadth of parasites' infectivity evolves, the nature of any associated costs, or the genetic basis of specialization. Here, we serially passage a granulosis virus on multiple inbred populations of its Plodia interpunctella host to explore the dynamics and outcomes of specialization. In particular, we collect time series of phenotypic and genetic data to explore the dynamics of host genotype specialization throughout the course of experimental evolution and examine two fitness components. We find that the Plodia interpunctella granulosis virus consistently evolves and increases in overall specialization, but that our two fitness components evolve independently such that lines can specialize in productivity or infectivity. Furthermore, we find that specialization in our experiment is a highly polygenic trait best explained by a combination of evolutionary mechanisms. These results are important for understanding the evolution of specialization in host-parasite interactions and its broader implications for co-existence, diversification, and infectious disease management.
Abstract.
Author URL.
2021
Guth S, Mollentze N, Renault K, Streicker DG, Visher E, Boots M, Brook CE (2021). Bats host the most virulent—but not the most dangerous—zoonotic viruses.
Alexander LW, Ben-Shachar R, Katzelnick LC, Kuan G, Balmaseda A, Harris E, Boots M (2021). Boosting can explain patterns of fluctuations of ratios of inapparent to symptomatic dengue virus infections.
Proc Natl Acad Sci U S A,
118(14).
Abstract:
Boosting can explain patterns of fluctuations of ratios of inapparent to symptomatic dengue virus infections.
Dengue is the most prevalent arboviral disease worldwide, and the four dengue virus (DENV) serotypes circulate endemically in many tropical and subtropical regions. Numerous studies have shown that the majority of DENV infections are inapparent, and that the ratio of inapparent to symptomatic infections (I/S) fluctuates substantially year-to-year. For example, in the ongoing Pediatric Dengue Cohort Study (PDCS) in Nicaragua, which was established in 2004, the I/S ratio has varied from 16.5:1 in 2006-2007 to 1.2:1 in 2009-2010. However, the mechanisms explaining these large fluctuations are not well understood. We hypothesized that in dengue-endemic areas, frequent boosting (i.e. exposures to DENV that do not lead to extensive viremia and result in a less than fourfold rise in antibody titers) of the immune response can be protective against symptomatic disease, and this can explain fluctuating I/S ratios. We formulate mechanistic epidemiologic models to examine the epidemiologic effects of protective homologous and heterologous boosting of the antibody response in preventing subsequent symptomatic DENV infection. We show that models that include frequent boosts that protect against symptomatic disease can recover the fluctuations in the I/S ratio that we observe, whereas a classic model without boosting cannot. Furthermore, we show that a boosting model can recover the inverse relationship between the number of symptomatic cases and the I/S ratio observed in the PDCS. These results highlight the importance of robust dengue control efforts, as intermediate dengue control may have the potential to decrease the protective effects of boosting.
Abstract.
Author URL.
Boots M, Childs D, Crossmore J, Tidbury H, Rudolf V (2021). Experimental evidence that local interactions select against selfish behaviour.
ECOLOGY LETTERS,
24(6), 1187-1192.
Author URL.
Ehrenberg AJ, Moehle EA, Brook CE, Doudna Cate AH, Witkowsky LB, Sachdeva R, Hirsh A, Barry K, Hamilton JR, Lin-Shiao E, et al (2021). Launching a saliva-based SARS-CoV-2 surveillance testing program on a university campus.
Ehrenberg AJ, Moehle EA, Brook CE, Cate AHD, Witkowsky LB, Sachdeva R, Hirsh A, Barry K, Hamilton JR, Lin-Shiao E, et al (2021). Launching a saliva-based SARS-CoV-2 surveillance testing program on a university campus. PLOS ONE, 16(5).
Lion S, Boots M, Sasaki A (2021). Multi-morph eco-evolutionary dynamics in structured populations.
Brook CE, Northrup GR, Ehrenberg AJ, IGI SARS-CoV-2 Testing Consortium, Doudna JA, Boots M (2021). Optimizing COVID-19 control with asymptomatic surveillance testing in a university environment.
medRxivAbstract:
Optimizing COVID-19 control with asymptomatic surveillance testing in a university environment.
The high proportion of transmission events derived from asymptomatic or presymptomatic infections make SARS-CoV-2, the causative agent in COVID-19, difficult to control through the traditional non-pharmaceutical interventions (NPIs) of symptom-based isolation and contact tracing. As a consequence, many US universities developed asymptomatic surveillance testing labs, to augment NPIs and control outbreaks on campus throughout the 2020-2021 academic year (AY); several of those labs continue to support asymptomatic surveillance efforts on campus in AY2021-2022. At the height of the pandemic, we built a stochastic branching process model of COVID-19 dynamics at UC Berkeley to advise optimal control strategies in a university environment. Our model combines behavioral interventions in the form of group size limits to deter superspreading, symptom-based isolation, and contact tracing, with asymptomatic surveillance testing. We found that behavioral interventions offer a cost-effective means of epidemic control: group size limits of six or fewer greatly reduce superspreading, and rapid isolation of symptomatic infections can halt rising epidemics, depending on the frequency of asymptomatic transmission in the population. Surveillance testing can overcome uncertainty surrounding asymptomatic infections, with the most effective approaches prioritizing frequent testing with rapid turnaround time to isolation over test sensitivity. Importantly, contact tracing amplifies population-level impacts of all infection isolations, making even delayed interventions effective. Combination of behavior-based NPIs and asymptomatic surveillance also reduces variation in daily case counts to produce more predictable epidemics. Furthermore, targeted, intensive testing of a minority of high transmission risk individuals can effectively control the COVID-19 epidemic for the surrounding population. Even in some highly vaccinated university settings in AY2021-2022, asymptomatic surveillance testing offers an effective means of identifying breakthrough infections, halting onward transmission, and reducing total caseload. We offer this blueprint and easy-to-implement modeling tool to other academic or professional communities navigating optimal return-to-work strategies.
Abstract.
Author URL.
Brook CE, Northrup GR, Ehrenberg AJ, IGI SARS-CoV-2 Testing Consortium, Doudna JA, Boots M (2021). Optimizing COVID-19 control with asymptomatic surveillance testing in a university environment.
Epidemics,
37Abstract:
Optimizing COVID-19 control with asymptomatic surveillance testing in a university environment.
The high proportion of transmission events derived from asymptomatic or presymptomatic infections make SARS-CoV-2, the causative agent in COVID-19, difficult to control through the traditional non-pharmaceutical interventions (NPIs) of symptom-based isolation and contact tracing. As a consequence, many US universities developed asymptomatic surveillance testing labs, to augment NPIs and control outbreaks on campus throughout the 2020-2021 academic year (AY); several of those labs continue to support asymptomatic surveillance efforts on campus in AY2021-2022. At the height of the pandemic, we built a stochastic branching process model of COVID-19 dynamics at UC Berkeley to advise optimal control strategies in a university environment. Our model combines behavioral interventions in the form of group size limits to deter superspreading, symptom-based isolation, and contact tracing, with asymptomatic surveillance testing. We found that behavioral interventions offer a cost-effective means of epidemic control: group size limits of six or fewer greatly reduce superspreading, and rapid isolation of symptomatic infections can halt rising epidemics, depending on the frequency of asymptomatic transmission in the population. Surveillance testing can overcome uncertainty surrounding asymptomatic infections, with the most effective approaches prioritizing frequent testing with rapid turnaround time to isolation over test sensitivity. Importantly, contact tracing amplifies population-level impacts of all infection isolations, making even delayed interventions effective. Combination of behavior-based NPIs and asymptomatic surveillance also reduces variation in daily case counts to produce more predictable epidemics. Furthermore, targeted, intensive testing of a minority of high transmission risk individuals can effectively control the COVID-19 epidemic for the surrounding population. Even in some highly vaccinated university settings in AY2021-2022, asymptomatic surveillance testing offers an effective means of identifying breakthrough infections, halting onward transmission, and reducing total caseload. We offer this blueprint and easy-to-implement modeling tool to other academic or professional communities navigating optimal return-to-work strategies.
Abstract.
Author URL.
Bartlett LJ, Boots M, Brosi BJ, de Roode JC, Delaplane KS, Hernandez CA, Wilfert L (2021). Persistent effects of management history on honeybee colony virus abundances.
J Invertebr Pathol,
179Abstract:
Persistent effects of management history on honeybee colony virus abundances.
Infectious diseases are a major threat to both managed and wild pollinators. One key question is how the movement or transplantation of honeybee colonies under different management regimes affects honeybee disease epidemiology. We opportunistically examined any persistent effect of colony management history following relocation by characterising the virus abundances of honeybee colonies from three management histories, representing different management histories: feral, low-intensity management, and high-intensity "industrial" management. The colonies had been maintained for one year under the same approximate 'common garden' condition. Colonies in this observational study differed in their virus abundances according to management history, with the feral population history showing qualitatively different viral abundance patterns compared to colonies from the two managed population management histories; for example, higher abundance of sacbrood virus but lower abundances of various paralysis viruses. Colonies from the high-intensity management history exhibited higher viral abundances for all viruses than colonies from the low-intensity management history. Our results provide evidence that management history has persistent impacts on honeybee disease epidemiology, suggesting that apicultural intensification could be majorly impacting on pollinator health, justifying much more substantial investigation.
Abstract.
Author URL.
Brook CE, Rozins C, Guth S, Boots M (2021). Reservoir host immunology and life history shape virulence evolution in zoonotic viruses.
Visher E, Uricchio L, Bartlett L, DeNamur N, Yarcan A, Alhassani D, Boots M (2021). The Evolution of Host Specialization in an Insect Pathogen.
Northrup GR, Parratt SR, Rozins C, Laine A-L, Boots M (2021). The Evolutionary Dynamics of Hyperparasites.
Visher E, Evensen C, Guth S, Lai E, Norfolk M, Rozins C, Sokolov NA, Sui M, Boots M (2021). The Three Ts of Pathogen Evolution During Zoonotic Emergence.
Bartlett LJ, Boots M (2021). The central role of host reproduction in determining the evolution of virulence in spatially structured populations.
J Theor Biol,
523Abstract:
The central role of host reproduction in determining the evolution of virulence in spatially structured populations.
A substantial body of work has shown that local transmission selects for less acute, 'prudent' parasites that have lower virulence and transmission rates. This is because parasite strains with higher transmission rates 'self-shade' due to a combination of genetic correlations (self: clustered related parasite strains compete for susceptible individuals) and ecological correlations (shade: infected individuals clustering and blocking transmission). However, the interaction of ecological and genetic correlations alongside higher order ecological effects such as patch extinctions means that spatial evolutionary effects can be nuanced; theory has predicted that a relatively small proportion of local infection can select for highest virulence, such that there is a humped relationship between the degree of local infection and the harm that parasites are selected to cause. Here, we examine the separate roles of the interaction scales of reproduction and infection in the context of different degrees of pathogenic castration in determining virulence evolution outcomes. Our key result is that, as long as there is significant reproduction from infected individuals, local infection always selects for lower virulence, and that the prediction that a small proportion of local infection can select for higher virulence only occurs for highly castrating pathogens. The results emphasize the importance of demography for evolutionary outcomes in spatially structured populations, but also show that the core prediction that parasites are prudent in space is reasonable for the vast majority of host-parasite interactions and mixing patterns in nature.
Abstract.
Author URL.
Sasaki A, Lion S, Boots M (2021). The impact of antigenic escape on the evolution of virulence.
Visher E, Evensen C, Guth S, Lai E, Norfolk M, Rozins C, Sokolov NA, Sui M, Boots M (2021). The three Ts of virulence evolution during zoonotic emergence.
Proc Biol Sci,
288(1956).
Abstract:
The three Ts of virulence evolution during zoonotic emergence.
There is increasing interest in the role that evolution may play in current and future pandemics, but there is often also considerable confusion about the actual evolutionary predictions. This may be, in part, due to a historical separation of evolutionary and medical fields, but there is a large, somewhat nuanced body of evidence-supported theory on the evolution of infectious disease. In this review, we synthesize this evolutionary theory in order to provide a framework for clearer understanding of the key principles. Specifically, we discuss the selection acting on zoonotic pathogens' transmission rates and virulence at spillover and during emergence. We explain how the direction and strength of selection during epidemics of emerging zoonotic disease can be understood by a three Ts framework: trade-offs, transmission, and time scales. Virulence and transmission rate may trade-off, but transmission rate is likely to be favoured by selection early in emergence, particularly if maladapted zoonotic pathogens have 'no-cost' transmission rate improving mutations available to them. Additionally, the optimal virulence and transmission rates can shift with the time scale of the epidemic. Predicting pathogen evolution, therefore, depends on understanding both the trade-offs of transmission-improving mutations and the time scales of selection.
Abstract.
Author URL.
Tellier A, Brown JK, Boots M, John S (2021). Theory of Host–Parasite Coevolution: from Ecology to Genomics. In (Ed) eLS, Wiley, 1-10.
2020
Best A, Jubrail J, Boots M, Dockrell D, Marriott H (2020). A mathematical model shows macrophages delay Staphylococcus aureus replication, but limitations in microbicidal capacity restrict bacterial clearance.
J Theor Biol,
497Abstract:
A mathematical model shows macrophages delay Staphylococcus aureus replication, but limitations in microbicidal capacity restrict bacterial clearance.
S. aureus is a leading cause of bacterial infection. Macrophages, the first line of defence in the human immune response, phagocytose and kill S. aureus but the pathogen can evade these responses. Therefore, the exact role of macrophages is incompletely defined. We develop a mathematical model of macrophage - S. aureus dynamics, built on recent experimental data. We demonstrate that, while macrophages may not clear infection, they significantly delay its growth and potentially buy time for recruitment of further cells. We find that macrophage killing is a major obstacle to controlling infection and ingestion capacity also limits the response. We find bistability such that the infection can be limited at low doses. Our combination of experimental data, mathematical analysis and model fitting provide important insights in to the early stages of S. aureus infections, showing macrophages play an important role limiting bacterial replication but can be overwhelmed with large inocula.
Abstract.
Author URL.
Brook CE, Boots M, Chandran K, Dobson AP, Drosten C, Graham AL, Grenfell BT, Müller MA, Ng M, Wang L-F, et al (2020). Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence.
eLife,
9Abstract:
Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence
Bats host virulent zoonotic viruses without experiencing disease. A mechanistic understanding of the impact of bats’ virus hosting capacities, including uniquely constitutive immune pathways, on cellular-scale viral dynamics is needed to elucidate zoonotic emergence. We carried out virus infectivity assays on bat cell lines expressing induced and constitutive immune phenotypes, then developed a theoretical model of our in vitro system, which we fit to empirical data. Best fit models recapitulated expected immune phenotypes for representative cell lines, supporting robust antiviral defenses in bat cells that correlated with higher estimates for within-host viral propagation rates. In general, heightened immune responses limit pathogen-induced cellular morbidity, which can facilitate the establishment of rapidly-propagating persistent infections within-host. Rapidly-transmitting viruses that have evolved with bat immune systems will likely cause enhanced virulence following emergence into secondary hosts with immune systems that diverge from those unique to bats.
Abstract.
Manley R, Temperton B, Boots M, Wilfert L (2020). Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees.
Mol Ecol,
29(2), 380-393.
Abstract:
Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees.
Typically, pathogens infect multiple host species. Such multihost pathogens can show considerable variation in their degree of infection and transmission specificity, which has important implications for potential disease emergence. Transmission of multihost pathogens can be driven by key host species and changes in such transmission networks can lead to disease emergence. We study two viruses that show contrasting patterns of prevalence and specificity in managed honeybees and wild bumblebees, black queen cell virus (BQCV) and slow bee paralysis virus (SBPV), in the context of the novel transmission route provided by the virus-vectoring Varroa destructor. Our key result is that viral communities and RNA virus genetic variation are structured by location, not host species or V. destructor presence. Interspecific transmission is pervasive with the same viral variants circulating between pollinator hosts in each location; yet, we found virus-specific host differences in prevalence and viral load. Importantly, V. destructor presence increases the prevalence in honeybees and, indirectly, in wild bumblebees, but in contrast to its impact on deformed wing virus (DWV), BQCV and SBPV viral loads are not increased by Varroa presence, and do not show genetic evidence of recent emergence. Effective control of Varroa in managed honeybee colonies is necessary to mitigate further disease emergence, and alleviate disease pressure on our vital wild bee populations. More generally, our results highlight the over-riding importance of geographical location to the epidemiological outcome despite the complexity of multihost-parasite interactions.
Abstract.
Author URL.
Guth S, Hanley KA, Althouse BM, Boots M (2020). Ecological processes underlying the emergence of novel enzootic cycles: Arboviruses in the neotropics as a case study. PLOS Neglected Tropical Diseases, 14(8).
Guth S, Hanley K, Althouse BM, Boots M (2020). Ecological processes underlying the emergence of novel enzootic cycles—arboviruses in the neotropics as a case study.
Roberts KE, Meaden S, Sharpe S, Kay S, Doyle T, Wilson D, Bartlett LJ, Paterson S, Boots M (2020). Resource quality determines the evolution of resistance and its genetic basis.
Molecular Ecology,
29(21), 4128-4142.
Abstract:
Resource quality determines the evolution of resistance and its genetic basis
AbstractParasites impose strong selection on their hosts, but the level of any evolved resistance may be constrained by the availability of resources. However, studies identifying the genomic basis of such resource‐mediated selection are rare, particularly in nonmodel organisms. Here, we investigated the role of nutrition in the evolution of resistance to a DNA virus (PiGV), and any associated trade‐offs in a lepidopteran pest species (Plodia interpunctella). Through selection experiments and whole‐genome resequencing, we identify genetic markers of resistance that vary between the nutritional environments during selection. We do not find consistent evolution of resistance in the presence of virus but rather see substantial variation among replicate populations. Resistance in a low‐nutrition environment is negatively correlated with growth rate, consistent with an established trade‐off between immunity and development, but this relationship is highly context dependent. Whole‐genome resequencing of the host shows that resistance mechanisms are likely to be highly polygenic and although the underlying genetic architecture may differ between high and low‐nutrition environments, similar mechanisms are commonly used. As a whole, our results emphasize the importance of the resource environment on influencing the evolution of resistance.
Abstract.
Smiley Evans T, Shi Z, Boots M, Liu W, Olival KJ, Xiao X, Vandewoude S, Brown H, Chen J-L, Civitello DJ, et al (2020). Synergistic China–US Ecological Research is Essential for Global Emerging Infectious Disease Preparedness. EcoHealth, 17(1), 160-173.
Cator LJ, Johnson LR, Mordecai EA, Moustaid FE, Smallwood TRC, LaDeau SL, Johansson MA, Hudson PJ, Boots M, Thomas MB, et al (2020). The Role of Vector Trait Variation in Vector-Borne Disease Dynamics. Frontiers in Ecology and Evolution, 8
Visher E, Boots M (2020). The problem of mediocre generalists: population genetics and eco-evolutionary perspectives on host breadth evolution in pathogens.
Proc Biol Sci,
287(1933).
Abstract:
The problem of mediocre generalists: population genetics and eco-evolutionary perspectives on host breadth evolution in pathogens.
Many of our theories for the generation and maintenance of diversity in nature depend on the existence of specialist biotic interactions which, in host-pathogen systems, also shape cross-species disease emergence. As such, niche breadth evolution, especially in host-parasite systems, remains a central focus in ecology and evolution. The predominant explanation for the existence of specialization in the literature is that niche breadth is constrained by trade-offs, such that a generalist is less fit on any particular environment than a given specialist. This trade-off theory has been used to predict niche breadth (co)evolution in both population genetics and eco-evolutionary models, with the different modelling methods providing separate, complementary insights. However, trade-offs may be far from universal, so population genetics theory has also proposed alternate mechanisms for costly generalism, including mutation accumulation. However, these mechanisms have yet to be integrated into eco-evolutionary models in order to understand how the mechanism of costly generalism alters the biological and ecological circumstances predicted to maintain specialism. In this review, we outline how population genetics and eco-evolutionary models based on trade-offs have provided insights for parasite niche breadth evolution and argue that the population genetics-derived mutation accumulation theory needs to be better integrated into eco-evolutionary theory.
Abstract.
Author URL.
Bartlett LJ, Visher E, Haro Y, Roberts KE, Boots M (2020). The target of selection matters: an established resistance-development-time negative genetic trade-off is not found when selecting on development time.
J Evol BiolAbstract:
The target of selection matters: an established resistance-development-time negative genetic trade-off is not found when selecting on development time.
Trade-offs are fundamental to evolutionary outcomes and play a central role in eco-evolutionary theory. They are often examined by experimentally selecting on one life-history trait and looking for negative correlations in other traits. For example, populations of the moth Plodia interpunctella selected to resist viral infection show a life-history cost with longer development times. However, we rarely examine whether the detection of such negative genetic correlations depends on the trait on which we select. Here, we examine a well-characterized negative genotypic trade-off between development time and resistance to viral infection in the moth Plodia interpunctella and test whether selection on a phenotype known to be a cost of resistance (longer development time) leads to the predicted correlated increase in resistance. If there is tight pleiotropic relationship between genes that determine development time and resistance underpinning this trade-off, we might expect increased resistance when we select on longer development time. However, we show that selecting for longer development time in this system selects for reduced resistance when compared to selection for shorter development time. This shows how phenotypes typically characterized by a trade-off can deviate from that trade-off relationship, and suggests little genetic linkage between the genes governing viral resistance and those that determine response to selection on the key life-history trait. Our results are important for both selection strategies in applied biological systems and for evolutionary modelling of host-parasite interactions.
Abstract.
Author URL.
2019
Brook CE, Boots M, Chandran K, Dobson AP, Drosten C, Graham AL, Grenfell BT, Müller MA, Ng M, Wang L-F, et al (2019). Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence.
Guth S, Visher E, Boots M, Brook CE (2019). Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal-human interface.
Philos Trans R Soc Lond B Biol Sci,
374(1782).
Abstract:
Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal-human interface.
Historically, efforts to assess 'zoonotic risk' have focused mainly on quantifying the potential for cross-species emergence of viruses from animal hosts. However, viruses clearly differ in relative burden, both in terms of morbidity and mortality (virulence) incurred and the capacity for sustained human-to-human transmission. Extending previously published databases, we delineated host and viral traits predictive of human mortality associated with viral spillover, viral capacity to transmit between humans following spillover and the probability of a given virus being zoonotic. We demonstrate that increasing host phylogenetic distance from humans positively correlates with human mortality but negatively correlates with human transmissibility, suggesting that the virulence induced by viruses emerging from hosts at high phylogenetic distance may limit capacity for human transmission. Our key result is that hosts most closely related to humans harbour zoonoses of lower impact in terms of morbidity and mortality, while the most distantly related hosts-in particular, order Chiroptera (bats)-harbour highly virulent zoonoses with a lower capacity for endemic establishment in human hosts. As a whole, our results emphasize the importance of understanding how zoonoses manifest in the human population and also highlight potential risks associated with multi-host transmission chains in spillover. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
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Author URL.
Manley R, Temperton B, Doyle T, Gates D, Hedges S, Boots M, Wilfert L (2019). Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees.
Ecol Lett,
22(8), 1306-1315.
Abstract:
Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees.
Novel transmission routes can directly impact the evolutionary ecology of infectious diseases, with potentially dramatic effect on host populations and knock-on effects on the wider host community. The invasion of Varroa destructor, an ectoparasitic viral vector in Western honeybees, provides a unique opportunity to examine how a novel vector affects disease epidemiology in a host community. This specialist honeybee mite vectors deformed wing virus (DWV), an important re-emerging honeybee pathogen that also infects wild bumblebees. Comparing island honeybee and wild bumblebee populations with and without V. destructor, we show that V. destructor drives DWV prevalence and titre in honeybees and sympatric bumblebees. Viral genotypes are shared across hosts, with the potentially more virulent DWV-B overtaking DWV-A in prevalence in a current epidemic. This demonstrates disease emergence across a host community driven by the acquisition of a specialist novel transmission route in one host, with dramatic community level knock-on effects.
Abstract.
Author URL.
Tanner E, White A, Lurz PWW, Gortázar C, Díez-Delgado I, Boots M (2019). The critical role of infectious disease in compensatory population growth in response to culling.
American Naturalist,
194(1), E1-E12.
Abstract:
The critical role of infectious disease in compensatory population growth in response to culling
Despite the ubiquity of disease in nature, the role that disease dynamics play in the compensatory growth response to harvesting has been ignored. We use a mathematical approach to show that harvesting can lead to compensatory growth due to a release from disease-induced mortality. Our findings imply that culling in systems that harbor virulent parasites can reduce disease prevalence and increase population density. Our models predict that this compensation occurs for a broad range of infectious disease characteristics unless the disease induces long-lasting immunity in hosts. Our key insight is that a population can be regulated at a similar density by disease or at reduced prevalence by a combination of culling and disease. We illustrate our predictions with a system-specific model representing wild boar tuberculosis infection, parameterized for central Spain, and find significant compensation to culling. Given that few wildlife diseases are likely to induce long-lived immunity, populations with virulent diseases may often be resilient to harvesting.
Abstract.
Iritani R, Visher E, Boots M (2019). The evolution of stage-specific virulence: Differential selection of parasites in juveniles.
Evol Lett,
3(2), 162-172.
Abstract:
The evolution of stage-specific virulence: Differential selection of parasites in juveniles.
The impact of infectious disease is often very different in juveniles and adults, but theory has focused on the drivers of stage-dependent defense in hosts rather than the potential for stage-dependent virulence evolution in parasites. Stage structure has the potential to be important to the evolution of pathogens because it exposes parasites to heterogeneous environments in terms of both host characteristics and transmission pathways. We develop a stage-structured (juvenile-adult) epidemiological model and examine the evolutionary outcomes of stage-specific virulence under the classic assumption of a transmission-virulence trade-off. We show that selection on virulence against adults remains consistent with the classic theory. However, the evolution of juvenile virulence is sensitive to both demography and transmission pathway with higher virulence against juveniles being favored either when the transmission pathway is assortative (juveniles preferentially interact together) and the juvenile stage is long, or in contrast when the transmission pathway is disassortative and the juvenile stage is short. These results highlight the potentially profound effects of host stage structure on determining parasite virulence in nature. This new perspective may have broad implications for both understanding and managing disease severity.
Abstract.
Author URL.
Roberts K, Meaden S, Sharpe S, Kay S, Doyle T, Wilson D, Bartlett LJ, Paterson S, Boots M (2019). The genomic basis of evolved virus resistance is dependent on environmental resources.
Bartlett L (2019). UBI MEL, IBI APES: on the evolutionary ecology of infectious diseases and intersections with apiculture.
Abstract:
UBI MEL, IBI APES: on the evolutionary ecology of infectious diseases and intersections with apiculture.
Infectious diseases shape almost every aspect of nature and society;
understanding the multitude of factors influencing infectious diseases is a critical goal of modern evolutionary ecology. This thesis explores this broad topic using theoretical and empirical approaches to understand the forces at work in infectious disease ecology and evolution, with application to the specific system of managed honeybees (Apis mellifera L.).
I demonstrate that a well-documented evolutionary trade-off governing pathogen resistance is both constitutive and genetic – critical for supporting assumptions made by mathematical theory. I go further to demonstrate that this trade-off breaks down when the action of selection is reversed, in that when the ‘cost of resistance’ phenotype is selective for, we do not incidentally select for higher resistance too. This is important for understanding genetic linkage of traits and downstream evolutionary modelling. I undertake theoretical modelling on the topic of spatial structure and how it affects pathogen evolution. In doing so I interrogate a critical assumption made in much of the prior theoretical body, showing that the effect of spatial structure on virulence is quantitatively changed when a core assumption concerning reproduction is relaxed, but is otherwise qualitatively robust.
I continue on the theme of spatial structuring and pathogens by developing novel theoretical models on how changing apicultural management alters honeybee population spatial structure, surprisingly leading to only marginal changes in pathogen burden. I stay on this topic to examine empirical data on honeybee colony viriomes in an observation experiment showing that colonies from very intensively managed. migratory backgrounds show elevated viral titres – critical for management and wild bee conservation. I synthesise that the honeybee system is our most informative natural experiment in showing that vectored pathogens are more virulent than directly transmitted
counterparts. I also show that outbreaking human epidemics (Zika virus) can threaten apiculture – and by extension livelihoods and agriculture.
Abstract.
Ashby B, Iritani R, Best A, White A, Boots M (2019). Understanding the role of eco-evolutionary feedbacks in host-parasite coevolution.
J Theor Biol,
464, 115-125.
Abstract:
Understanding the role of eco-evolutionary feedbacks in host-parasite coevolution.
It is widely recognised that eco-evolutionary feedbacks can have important implications for evolution. However, many models of host-parasite coevolution omit eco-evolutionary feedbacks for the sake of simplicity, typically by assuming the population sizes of both species are constant. It is often difficult to determine whether the results of these models are qualitatively robust if eco-evolutionary feedbacks are included. Here, by allowing interspecific encounter probabilities to depend on population densities without otherwise varying the structure of the models, we provide a simple method that can test whether eco-evolutionary feedbacks per se affect evolutionary outcomes. Applying this approach to explicit genetic and quantitative trait models from the literature, our framework shows that qualitative changes to the outcome can be directly attributable to eco-evolutionary feedbacks. For example, shifting the dynamics between stable monomorphism or polymorphism and cycling, as well as changing the nature of the cycles. Our approach, which can be readily applied to many different models of host-parasite coevolution, offers a straightforward method for testing whether eco-evolutionary feedbacks qualitatively change coevolutionary outcomes.
Abstract.
Author URL.
2018
Carlson CJ, Dougherty E, Boots M, Getz W, Ryan SJ (2018). Consensus and conflict among ecological forecasts of Zika virus outbreaks in the United States. Scientific Reports, 8(1).
Bartlett LJ, Carlson CJ, Boots M (2018). Identifying regions of risk to honey bees from Zika vector control in the USA.
Journal of Apicultural Research,
57(5), 709-719.
Abstract:
Identifying regions of risk to honey bees from Zika vector control in the USA
Managed honey bees are a crucial component of many countries’ agricultural systems. Critically, it is now well established that honey bees are faced with multiple threats, and therefore, it is important that we determine and mitigate new threats. The emergence of Zika virus has introduced the new threat of insecticidal mosquito control leading to honey bee losses, with demand from beekeepers for a comprehensive risk assessment to help mitigate losses. Here, we present novel estimates of county-level honey bee colony densities across the USA and combine these new data with different projections of Zika virus suitability to assess the magnitude of this risk. We find that up to 13% of colonies can reasonably be expected to experience elevated risk of damaging pesticide exposure, according to interpretation of current Zika virus projections. We show a significant positive correlation between areas of Zika suitability and honey bee colony density. Increased risk of colony loss to pesticides are found in the South-East, Gulf Coast, Florida, and the California Central Valley. We highlight certain states which are better placed to mitigate threats, recommending other states look towards these schemes to protect apiculture from both government and commercial pesticide application.
Abstract.
Díez-Delgado I, Sevilla IA, Romero B, Tanner E, Barasona JA, White AR, Lurz PWW, Boots M, de la Fuente J, Dominguez L, et al (2018). Impact of piglet oral vaccination against tuberculosis in endemic free-ranging wild boar populations.
Preventive Veterinary Medicine,
155, 11-20.
Abstract:
Impact of piglet oral vaccination against tuberculosis in endemic free-ranging wild boar populations
The Eurasian wild boar (Sus scrofa) is the main wild reservoir of the Mycobacterium tuberculosis complex in Mediterranean woodlands and a key risk factor for cattle tuberculosis (TB) breakdowns. Wild boar vaccination therefore has the potential to be a valuable tool for TB control. We tested two orally delivered vaccines, heat-inactivated Mycobacterium bovis (IV) and BCG, in four sites (two per vaccine type: one Managed and one Natural or unmanaged) during four years. TB was also monitored in 15 unvaccinated sites (spatial control), as well as in all sites from one year prior to intervention (temporal control). The rationale is that by vaccinating 2–6 month old wild boar piglets we can reduce disease at the population level during the study period. This is achievable due to the fast turnover of wild boar populations. Vaccine baits were deployed using selective piglet feeders and this method proved highly successful with uptake rates of 50 to 74% in Natural sites and 89 to 92% in Managed sites. This is relevant for the potential delivery of vaccines to control other diseases, too. Local wild boar TB prevalence at the beginning of the study was already high ranging from 50 to 100%. TB prevalence increased in unvaccinated sites (6%), while a significant decline occurred in the Managed IV site (34%). Changes recorded in the remaining sites were not significant. The short-term impact of vaccination observed in the field was complemented by mathematical modelling, representative of the field system, which examined the long-term impact and showed that vaccination of piglets reduced prevalence and increased abundance at the population level. We conclude that IV could become part of integrated TB control schemes, although its application must be tailored for each specific site.
Abstract.
Bartlett LJ, Rozins C, Brosi BJ, Delaplane KS, de Roode JC, White A, Wilfert L, Boots M (2018). Industrial bees: when agricultural intensification doesn’t impact local disease prevalence.
Cator LJ, Johnson LR, Mordecai EA, Moustaid FE, Smallwood TRC, LaDeau SL, Johansson MA, Hudson PJ, Boots M, Thomas MB, et al (2018). More than a flying syringe: Using functional traits in vector-borne disease research.
Rozins C, Silk MJ, Croft DP, Delahay RJ, Hodgson DJ, McDonald RA, Weber N, Boots M (2018). Social structure contains epidemics and regulates individual roles in disease transmission in a group-living mammal.
Ecology and Evolution,
8(23), 12044-12055.
Abstract:
Social structure contains epidemics and regulates individual roles in disease transmission in a group-living mammal
Population structure is critical to infectious disease transmission. As a result, theoretical and empirical contact network models of infectious disease spread are increasingly providing valuable insights into wildlife epidemiology. Analyzing an exceptionally detailed dataset on contact structure within a high-density population of European badgers Meles meles, we show that a modular contact network produced by spatially structured stable social groups, lead to smaller epidemics, particularly for infections with intermediate transmissibility. The key advance is that we identify considerable variation among individuals in their role in disease spread, with these new insights made possible by the detail in the badger dataset. Furthermore, the important impacts on epidemiology are found even though the modularity of the Badger network is much lower than the threshold that previous work suggested was necessary. These findings reveal the importance of stable social group structure for disease dynamics with important management implications for socially structured populations.
Abstract.
Boots M, Best A (2018). The evolution of constitutive and induced defences to infectious disease.
Proc Biol Sci,
285(1883).
Abstract:
The evolution of constitutive and induced defences to infectious disease.
In response to infectious disease, hosts typically mount both constitutive and induced defences. Constitutive defence prevents infection in the first place, while induced defence typically shortens the infectious period. The two routes to defence, therefore, have very different implications not only to individuals but also to the epidemiology of the disease. Moreover, the costs of constitutive defences are likely to be paid even in the absence of disease, while induced defences are likely to incur the most substantial costs when they are used in response to infection. We examine theoretically the evolutionary implications of these fundamental differences. A key result is that high virulence in the parasite typically selects for higher induced defences even if they result in immunopathology leading to very high disease mortality. Disease impacts on fecundity are critical to the relative investment in constitutive and induced defence with important differences found when parasites castrate their hosts. The trade-off between constitutive and induced defence has been cited as a cause of the diversity in defence, but we show that the trade-off alone is unlikely to lead to diversity. Our models provide a framework to examine relative investment in different defence components both experimentally and in the field.
Abstract.
Author URL.
Iritani R, Visher E, Boots M (2018). The evolution of stage-specific virulence: differential selection of parasites in juveniles.
2017
Carlson CJ, Dougherty E, Boots M, Getz W, Ryan S (2017). Consensus and conflict among ecological forecasts of Zika virus outbreaks in the United States.
Brosi BJ, Delaplane KS, Boots M, de Roode JC (2017). Ecological and evolutionary approaches to managing honeybee disease. Nature Ecology & Evolution, 1(9), 1250-1262.
Donnelly R, White A, Boots M (2017). Host lifespan and the evolution of resistance to multiple parasites.
J Evol Biol,
30(3), 561-570.
Abstract:
Host lifespan and the evolution of resistance to multiple parasites.
Hosts are typically challenged by multiple parasites, but to date theory on the evolution of resistance has mainly focused on single infections. We develop a series of models that examine the impact of multiple parasites on the evolution of resistance under the assumption that parasites coexist at the host population scale as a consequence of superinfection. In this way, we are able to explicitly examine the impact of ecological dynamics on the evolutionary outcome. We use our models to address a key question of how host lifespan affects investment in resistance to multiple parasites. We show that investment in costly resistance depends on the specificity of the immune response and on whether or not the focal parasite leads to more acute infection than the co-circulating parasite. A key finding is that investment in resistance always increases as the immune response becomes more general independently of whether it is the focal or the co-circulating parasite that exploits the host most aggressively. Long-lived hosts always invest more than short-lived hosts in both general resistance and resistance that is specific to relatively acute focal parasites. However, for specific resistance to parasites that are less acute than co-circulating parasites it is the short-lived hosts that are predicted to invest most. We show that these results apply whatever the mode of defence, that is whether it is through avoidance or through increased recovery, with or without acquired immunity, or through acquired immunity itself. As a whole, our results emphasize the importance of considering multiple parasites in determining optimal immune investment in eco-evolutionary systems.
Abstract.
Author URL.
Best A, Ashby B, White A, Bowers R, Buckling A, Koskella B, Boots M (2017). Host-parasite fluctuating selection in the absence of specificity.
Proc Biol Sci,
284(1866).
Abstract:
Host-parasite fluctuating selection in the absence of specificity.
Fluctuating selection driven by coevolution between hosts and parasites is important for the generation of host and parasite diversity across space and time. Theory has focused primarily on infection genetics, with highly specific 'matching-allele' frameworks more likely to generate fluctuating selection dynamics (FSD) than 'gene-for-gene' (generalist-specialist) frameworks. However, the environment, ecological feedbacks and life-history characteristics may all play a role in determining when FSD occurs. Here, we develop eco-evolutionary models with explicit ecological dynamics to explore the ecological, epidemiological and host life-history drivers of FSD. Our key result is to demonstrate for the first time, to our knowledge, that specificity between hosts and parasites is not required to generate FSD. Furthermore, highly specific host-parasite interactions produce unstable, less robust stochastic fluctuations in contrast to interactions that lack specificity altogether or those that vary from generalist to specialist, which produce predictable limit cycles. Given the ubiquity of ecological feedbacks and the variation in the nature of specificity in host-parasite interactions, our work emphasizes the underestimated potential for host-parasite coevolution to generate fluctuating selection.
Abstract.
Author URL.
Ashby B, Boots M (2017). Multi-mode fluctuating selection in host-parasite coevolution.
Ecol Lett,
20(3), 357-365.
Abstract:
Multi-mode fluctuating selection in host-parasite coevolution.
Understanding fluctuating selection is important for our understanding of patterns of spatial and temporal diversity in nature. Host-parasite theory has classically assumed fluctuations either occur between highly specific genotypes (matching allele: MA) or from specialism to generalism (gene-for-gene: GFG). However, while MA can only generate one mode of fluctuating selection, we show that GFG can in fact produce both rapid 'within-range' fluctuations (among genotypes with identical levels of investment but which specialise on different subsets of the population) and slower cycling 'between ranges' (different levels of investment), emphasising that MA is a subset of GFG. Our findings closely match empirical observations, although sampling rates need to be high to detect these novel dynamics empirically. Within-range cycling is an overlooked process by which fluctuating selection can occur in nature, suggesting that fluctuating selection may be a more common and important process than previously thought in generating and maintaining diversity.
Abstract.
Author URL.
Brosi BJ, Delaplane KS, Boots M, Roode JC (2017). Publisher Correction: Ecological and evolutionary approaches to managing honeybee disease. Nature Ecology & Evolution, 2(1), 196-196.
Lynch PA, Boots M (2017). SAFE INDOORS: CHEAP, SUSTAINABLE SPATIAL REPELLENTS TO COMBAT RESISTANCE AND KEEP MALARIA VECTORS OUT OF HOMES.
Author URL.
Silk MJ, Croft DP, Delahay RJ, Hodgson DJ, Weber N, Boots M, Mcdonald RA (2017). The application of statistical network models in disease research.
Methods in Ecology and EvolutionAbstract:
The application of statistical network models in disease research
© 2017 British Ecological Society.Host social structure is fundamental to how infections spread and persist, and so the statistical modelling of static and dynamic social networks provides an invaluable tool to parameterise realistic epidemiological models. We present a practical guide to the application of network modelling frameworks for hypothesis testing related to social interactions and epidemiology, illustrating some approaches with worked examples using data from a population of wild European badgers Meles meles naturally infected with bovine tuberculosis. Different empirical network datasets generate particular statistical issues related to non-independence and sampling constraints. We therefore discuss the strengths and weaknesses of modelling approaches for different types of network data and for answering different questions relating to disease transmission. We argue that statistical modelling frameworks designed specifically for network analysis offer great potential in directly relating network structure to infection. They have the potential to be powerful tools in analysing empirical contact data used in epidemiological studies, but remain untested for use in networks of spatio-temporal associations. As a result, we argue that developments in the statistical analysis of empirical contact data are critical given the ready availability of dynamic network data from bio-logging studies. Furthermore, we encourage improved integration of statistical network approaches into epidemiological research to facilitate the generation of novel modelling frameworks and help extend our understanding of disease transmission in natural populations.
Abstract.
Best A, White A, Boots M (2017). The evolution of host defence when parasites impact reproduction.
Evolutionary Ecology Research,
18(4), 393-409.
Abstract:
The evolution of host defence when parasites impact reproduction
Question: How does the evolution of host defences to parasitism depend on the level of disease-induced sterility? Mathematical methods: Evolutionary invasion analysis (adaptive dynamics) applied to susceptible-infected host-parasite model. Key assumptions: Hosts can evolve defence through avoidance (lower transmission), clearance (higher recovery) or tolerance (lower virulence), in isolation or simultaneously, at a cost to their reproductive rate. Separation of ecological and evolutionary timescales and mutations of small phenotypic effect. Conclusions: Avoidance and clearance are maximized when sterility is high, but tolerance is greatest when sterility is low. However, when clearance and tolerance co-evolve there is greater tolerance at high sterility, as this boosts the effectiveness of clearance. Patterns of investment along other environmental gradients can change as the level of sterility changes. Evolutionary branching to co-existence in avoidance and clearance is most likely when sterility is high.
Abstract.
2016
Wilfert L, Long G, Leggett H, Schmid-Hempel P, Butlin R, Martin SJM, Boots M (2016). Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites.
ScienceAbstract:
Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites
Deformed Wing Virus (DWV) and its vector Varroa destructor, which emerged last century, are a major threat to the world’s honeybees. While Varroa’s dramatic impacts on colony-level DWV epidemiology is evident, we have little understanding of wider DWV epidemiology and the role that Varroa has played in its global spread. A phylogeographic analysis shows that DWV is globally distributed in honeybees, having recently spread from a common source, the European honeybee Apis mellifera. DWV shows epidemic growth and transmission that is predominantly mediated by European and North American honeybee populations and driven by trade and movement of honeybee colonies. DWV is now an important re-emerging pathogen of honeybees undergoing a worldwide man-made epidemic, fuelled by the novel direct transmission route provided by the Varroa mite.
Abstract.
Boots M (2016). Environmental determinants of resistance: Theoretical models and Plodia interpunctella vs PiGV. 2016 International Congress of Entomology.
Grunnill M, Boots M (2016). How Important is Vertical Transmission of Dengue Viruses by Mosquitoes (Diptera: Culicidae)?.
J Med Entomol,
53(1), 1-19.
Abstract:
How Important is Vertical Transmission of Dengue Viruses by Mosquitoes (Diptera: Culicidae)?
Vertical transmission of dengue viruses by mosquitoes was discovered at the end of the late 1970s and has been suggested to be a means by which these viruses persist. However, it is unclear how widespread it is in nature, and its importance in the epidemiology of this disease is still debated. Here, we review the literature on vertical transmission and discuss its role in dengue's epidemiology and control. We conclude that given the number of studies that failed to find evidence of vertical transmission, as well as mathematical models and its mechanistic basis, it is unlikely that vertical transmission is important for the epidemiological persistence of dengue viruses. A combination of asymptomatic infection in humans and movement of people are likely to be more important determinants of dengue's persistence. We argue, however, that there may be some need for further research into the prevalence of dengue viruses in desiccated, as well as diapausing, eggs and the role of horizontal transmission through larval cannibalism.
Abstract.
Author URL.
White A, Lurz PWW, Bryce J, Tonkin M, Ramoo K, Bamforth L, Jarrott A, Boots M (2016). Modelling disease spread in real landscapes: Squirrelpox spread in southern Scotland as a case study.
Hystrix,
27(1).
Abstract:
Modelling disease spread in real landscapes: Squirrelpox spread in southern Scotland as a case study
There is increasing evidence that invading species can gain an advantage over native species by introducing novel disease. A clear understanding of the role of disease in the expansion of introduced and invading species is therefore essential for the conservation of native species. In this study we focus on the case study system of the UK red and grey squirrel system in which disease-mediated competition has facilitated the replacement of red squirrels by greys. We modify a deterministic model of the squirrel system in which the competition and infection dynamics are well understood to produce a stochastic model which includes a realistic representation of the heterogeneous habitat in Southern Scotland. The model is used to examine the potential spread of infection (squirrelpox virus) through the squirrel system and to examine the impact of conservation measures that control grey squirrel numbers in an attempt to contain disease spread. The results have direct implications for conservation management and we discuss how they have helped shape current and future policy for red squirrel conservation in Scotland. The methods in this study can be readily adapted to represent different systems and since the stochastic population and disease dynamics are underpinned by classical deterministic modelling frameworks the results are applicable in general.
Abstract.
Jones HE, White A, Geddes N, Clavey P, Farries J, Dearnley T, Boots M, Lurz PWW (2016). Modelling the impact of forest design plans on an endangered mammal species: the eurasian red squirrel.
Hystrix,
27(1).
Abstract:
Modelling the impact of forest design plans on an endangered mammal species: the eurasian red squirrel
The Eurasian red squirrel (Sciurus vulgaris) is under threat in the UK from the introduced North American grey squirrel. National measures to save the species include large conifer forest reserves where management encompasses measures to bolster the native species. However, forests are multipurpose environments and foresters have to balance different timber production, amenity and conservation objectives. We present a mathematical modelling framework that examines the impacts of potential felling and restocking plans for two reserves, Kidland and Uswayford forests, in northern England. In collaboration with forest managers, we employed an iterative process that used the model to assess four forest design plans (felling and restocking scenarios) with the aim of improving red squirrel population viability. Overall, the model predicted that extinction in both forests at the same time was rare, but high in Uswayford (84%) alone. Survival could be drastically increased (from 16% to 70%) by felling and restocking adjustments, and improving dispersal between the two adjacent forests. This study provides an exemplar of how modelling can have a direct input to land management to help managers objectively balance the differing pressures of multipurpose forestry.
Abstract.
van Houte S, Ekroth AKE, Broniewski JM, Chabas H, Ashby B, Bondy-Denomy J, Gandon S, Boots M, Paterson S, Buckling A, et al (2016). The diversity-generating benefits of a prokaryotic adaptive immune system.
Nature,
532(7599), 385-388.
Abstract:
The diversity-generating benefits of a prokaryotic adaptive immune system.
Prokaryotic CRISPR-Cas adaptive immune systems insert spacers derived from viruses and other parasitic DNA elements into CRISPR loci to provide sequence-specific immunity. This frequently results in high within-population spacer diversity, but it is unclear if and why this is important. Here we show that, as a result of this spacer diversity, viruses can no longer evolve to overcome CRISPR-Cas by point mutation, which results in rapid virus extinction. This effect arises from synergy between spacer diversity and the high specificity of infection, which greatly increases overall population resistance. We propose that the resulting short-lived nature of CRISPR-dependent bacteria-virus coevolution has provided strong selection for the evolution of sophisticated virus-encoded anti-CRISPR mechanisms.
Abstract.
Author URL.
Su M, Boots M (2016). The impact of resource quality on the evolution of virulence in spatially heterogeneous environments. Journal of Theoretical Biology, 416, 1-7.
Pastok D, Hoare MJ, Ryder JJ, Boots M, Knell RJ, Atkinson D, Hurst GDD (2016). The role of host phenology in determining the incidence of an insect sexually transmitted infection.
Oikos,
125(5), 636-643.
Abstract:
The role of host phenology in determining the incidence of an insect sexually transmitted infection
Changes in the timing of life history events within the year alter the degree to which the activity patterns of different species coincide, making the dynamics of interspecific interactions sensitive to the phenology of the interacting parties. For parasites, the availability of suitable hosts to infect represents a crucial determinant of dynamics, and changes in the host (and parasite) phenology may thus alter disease epidemiology and the conditions for disease maintenance. We tested the hypothesis that the incidence of a sexually transmitted mite infection, Coccipolipus hippodamiae, in Adalia bipunctata ladybird beetles in Sweden was determined by host phenology, namely presence/absence of sexual contact between cohorts of the host. We observed that the pattern of mite presence/absence across Swedish A. bipunctata populations was highly reproducible between years, implying a persistent biological/ecological basis underlying the incidence. Further, ladybirds from populations where the mite was absent were able to acquire mites during copulation, develop a mite infection, and transmit infection onward, indicating an ecological (rather than biological) driver of mite incidence. Observations of ladybird phenology in natural populations provided evidence of sexual contact between overwintered and new cohort adults in populations where the mite was present. In contrast, new cohort ladybirds in the two northern Swedish populations where the mite was not present had not had sexual contact with the overwintered generation, creating a 'hard stop' to mite transmission. We conclude that variation in host phenology may be an important driver of the incidence of sexually transmitted infections (STIs) by determining the presence/absence of sexual contact between generations. More generally, we hypothesize that sensitivity to variation in host phenology will be highest for parasites like STIs that infect one host species, one host life stage and are directly transmitted on contact between host individuals.
Abstract.
Lynch PA, Boots M (2016). Using evolution to generate sustainable malaria control with spatial repellents.
eLife,
5(OCTOBER2016).
Abstract:
Using evolution to generate sustainable malaria control with spatial repellents
© Lynch and Boots. Evolution persistently undermines vector control programs through insecticide resistance. Here we propose a novel strategy which instead exploits evolution to generate and sustain new control tools. Effective spatial repellents are needed to keep vectors out of houses. Our approach generates such new repellents by combining a high-toxicity insecticide with a candidate repellent initially effective against only part of the vector population. By killing mosquitoes that enter treated properties the insecticide selects for vector phenotypes deflected by the repellent, increasing efficacy of the repellent against the target vector population and in turn protecting the insecticide against the spread of insecticide resistance. Using such evolved spatial repellents offers an evolutionarily sustainable, ‘double-dip’ system of disease control c ombining mortality and repellence. We formalize this idea using models which explore vector population genetics and disease transmission probabilities and show that using evolved spatial repellents is theoretically achievable, effective and sustainable.
Abstract.
2015
Ashby B, Boots M (2015). Coevolution of parasite virulence and host mating strategies.
Proc Natl Acad Sci U S A,
112(43), 13290-13295.
Abstract:
Coevolution of parasite virulence and host mating strategies.
Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasite-mediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.
Abstract.
Author URL.
Manley R, Boots M, Wilfert L (2015). Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors.
J Appl Ecol,
52, 331-340.
Author URL.
Westra ER, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM, Best A, Bondy-Denomy J, Davidson A, Boots M, Buckling A, et al (2015). Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense.
Curr Biol,
25(8), 1043-1049.
Abstract:
Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense.
In the face of infectious disease, organisms evolved a range of defense mechanisms, with a clear distinction between those that are constitutive (always active) and those that are inducible (elicited by parasites). Both defense strategies have evolved from each other, but we lack an understanding of the conditions that favor one strategy over the other. While it is hard to generalize about their degree of protection, it is possible to make generalizations about their associated fitness costs, which are commonly detected. By definition, constitutive defenses are always "on," and are therefore associated with a fixed cost, independent of parasite exposure. Inducible defenses, on the other hand, may lack costs in the absence of parasites but become costly when defense is elicited through processes such as immunopathology. Bacteria can evolve constitutive defense against phage by modification/masking of surface receptors, which is often associated with reduced fitness in the absence of phage. Bacteria can also evolve inducible defense using the CRISPR-Cas (clustered regularly interspaced short palindromic repeat, CRISPR associated) immune system, which is typically elicited upon infection. CRISPR-Cas functions by integrating phage sequences into CRISPR loci on the host genome. Upon re-infection, CRISPR transcripts guide cleavage of phage genomes. In nature, both mechanisms are important. Using a general theoretical model and experimental evolution, we tease apart the mechanism that drives their evolution and show that infection risk determines the relative investment in the two arms of defense.
Abstract.
Author URL.
Westra ER, Van houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM, Best A, Bondy-Denomy J, Davidson A, Boots M, Buckling A, et al (2015). Parasite exposure drives selective evolution of constitutive versus inducible defense.
Current Biology,
25(8), 1043-1049.
Abstract:
Parasite exposure drives selective evolution of constitutive versus inducible defense
Summary in the face of infectious disease, organisms evolved a range of defense mechanisms, with a clear distinction between those that are constitutive (always active) and those that are inducible (elicited by parasites) [1]. Both defense strategies have evolved from each other [2], but we lack an understanding of the conditions that favor one strategy over the other. While it is hard to generalize about their degree of protection, it is possible to make generalizations about their associated fitness costs, which are commonly detected [3-5]. By definition, constitutive defenses are always "on," and are therefore associated with a fixed cost, independent of parasite exposure [4, 5]. Inducible defenses, on the other hand, may lack costs in the absence of parasites but become costly when defense is elicited [6] through processes such as immunopathology [7]. Bacteria can evolve constitutive defense against phage by modification/masking of surface receptors [8, 9], which is often associated with reduced fitness in the absence of phage [10]. Bacteria can also evolve inducible defense using the CRISPR-Cas (clustered regularly interspaced short palindromic repeat, CRISPR associated) immune system [11], which is typically elicited upon infection [12-14]. CRISPR-Cas functions by integrating phage sequences into CRISPR loci on the host genome [15]. Upon re-infection, CRISPR transcripts guide cleavage of phage genomes [16-20]. In nature, both mechanisms are important [21, 22]. Using a general theoretical model and experimental evolution, we tease apart the mechanism that drives their evolution and show that infection risk determines the relative investment in the two arms of defense.
Abstract.
Hesse E, Best A, Boots M, Hall AR, Buckling A (2015). Spatial heterogeneity lowers rather than increases host-parasite specialization.
Journal of Evolutionary Biology,
28(9), 1682-1690.
Abstract:
Spatial heterogeneity lowers rather than increases host-parasite specialization
Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host-parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ϕ{symbol}2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host-parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host-parasite specialization.
Abstract.
Hesse E, Best A, Boots M, Hall AR, Buckling A (2015). Spatial heterogeneity lowers rather than increases host-parasite specialization.
J Evol Biol,
28(9), 1682-1690.
Abstract:
Spatial heterogeneity lowers rather than increases host-parasite specialization.
Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host-parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ϕ2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host-parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host-parasite specialization.
Abstract.
Author URL.
Boots M (2015). The Need for Evolutionarily Rational Disease Interventions: Vaccination can Select for Higher Virulence.
PLoS Biol,
13(8).
Abstract:
The Need for Evolutionarily Rational Disease Interventions: Vaccination can Select for Higher Virulence.
There is little doubt evolution has played a major role in preventing the control of infectious disease through antibiotic and insecticide resistance, but recent theory suggests disease interventions such as vaccination may lead to evolution of more harmful parasites. A new study published in PLOS Biology by Andrew Read and colleagues shows empirically that vaccination against Marek's disease has favored higher virulence; without intervention, the birds die too quickly for any transmission to occur, but vaccinated hosts can both stay alive longer and shed the virus. This is an elegant empirical demonstration of how evolutionary theory can predict potentially dangerous responses of infectious disease to human interventions.
Abstract.
Author URL.
Donnelly R, White A, Boots M (2015). The epidemiological feedbacks critical to the evolution of host immunity.
Journal of Evolutionary Biology,
28(11), 2042-2053.
Abstract:
The epidemiological feedbacks critical to the evolution of host immunity
We examine in detail how epidemiological feedbacks combine with costs and benefits to determine the evolution of resistance by systematically analysing continuously stable strategies (CSS) for different host-parasite frameworks. The mode of resistance (innate versus acquired), the nature of the host (i.e. life-history and immunological memory) and the nature of the disease (effects on fertility or mortality) all impact on the feedbacks that are critical to the evolution of resistance. By identifying relationships between CSS investment and the underlying epidemiological feedback for each mode of resistance in each framework, we distil complex feedbacks into simple combinations of selection pressures. When the parasite does not affect fertility, CSS investment reflects only the benefit of resistance and we explain why this is markedly different for innate and acquired resistance. If infection has no effect on host fertility, CSS investment in acquired immunity increases with the square of disease prevalence. While in contrast for evolving innate resistance, CSS investment is greatest at intermediate prevalence. When disease impacts fertility, only a fraction of the host population reproduce, and this introduces new ecological feedbacks to both the cost of resistance and the damage from infection. The multiple feedbacks in this case lead to the alternative result that the higher the abundance of infecteds, the higher the investment in innate resistance. A key insight is that maximal investment occurs at intermediate lifespans in a range of different host-parasite interactions, but for disparate reasons which can only be understood by a detailed analysis of the feedbacks. We discuss the extension of our approach to structured host populations and parasite community dynamics.
Abstract.
Donnelly R, White A, Boots M (2015). The epidemiological feedbacks critical to the evolution of host immunity.
J Evol Biol,
28(11), 2042-2053.
Abstract:
The epidemiological feedbacks critical to the evolution of host immunity.
We examine in detail how epidemiological feedbacks combine with costs and benefits to determine the evolution of resistance by systematically analysing continuously stable strategies (CSS) for different host-parasite frameworks. The mode of resistance (innate versus acquired), the nature of the host (i.e. life-history and immunological memory) and the nature of the disease (effects on fertility or mortality) all impact on the feedbacks that are critical to the evolution of resistance. By identifying relationships between CSS investment and the underlying epidemiological feedback for each mode of resistance in each framework, we distil complex feedbacks into simple combinations of selection pressures. When the parasite does not affect fertility, CSS investment reflects only the benefit of resistance and we explain why this is markedly different for innate and acquired resistance. If infection has no effect on host fertility, CSS investment in acquired immunity increases with the square of disease prevalence. While in contrast for evolving innate resistance, CSS investment is greatest at intermediate prevalence. When disease impacts fertility, only a fraction of the host population reproduce, and this introduces new ecological feedbacks to both the cost of resistance and the damage from infection. The multiple feedbacks in this case lead to the alternative result that the higher the abundance of infecteds, the higher the investment in innate resistance. A key insight is that maximal investment occurs at intermediate lifespans in a range of different host-parasite interactions, but for disparate reasons which can only be understood by a detailed analysis of the feedbacks. We discuss the extension of our approach to structured host populations and parasite community dynamics.
Abstract.
Author URL.
2014
McVicker G, Prajsnar TK, Williams A, Wagner NL, Boots M, Renshaw SA, Foster SJ (2014). Clonal expansion during Staphylococcus aureus infection dynamics reveals the effect of antibiotic intervention.
PLoS Pathog,
10(2).
Abstract:
Clonal expansion during Staphylococcus aureus infection dynamics reveals the effect of antibiotic intervention.
To slow the inexorable rise of antibiotic resistance we must understand how drugs impact on pathogenesis and influence the selection of resistant clones. Staphylococcus aureus is an important human pathogen with populations of antibiotic-resistant bacteria in hospitals and the community. Host phagocytes play a crucial role in controlling S. aureus infection, which can lead to a population "bottleneck" whereby clonal expansion of a small fraction of the initial inoculum founds a systemic infection. Such population dynamics may have important consequences on the effect of antibiotic intervention. Low doses of antibiotics have been shown to affect in vitro growth and the generation of resistant mutants over the long term, however whether this has any in vivo relevance is unknown. In this work, the population dynamics of S. aureus pathogenesis were studied in vivo using antibiotic-resistant strains constructed in an isogenic background, coupled with systemic models of infection in both the mouse and zebrafish embryo. Murine experiments revealed unexpected and complex bacterial population kinetics arising from clonal expansion during infection in particular organs. We subsequently elucidated the effect of antibiotic intervention within the host using mixed inocula of resistant and sensitive bacteria. Sub-curative tetracycline doses support the preferential expansion of resistant microorganisms, importantly unrelated to effects on growth rate or de novo resistance acquisition. This novel phenomenon is generic, occurring with methicillin-resistant S. aureus (MRSA) in the presence of β-lactams and with the unrelated human pathogen Pseudomonas aeruginosa. The selection of resistant clones at low antibiotic levels can result in a rapid increase in their prevalence under conditions that would previously not be thought to favor them. Our results have key implications for the design of effective treatment regimes to limit the spread of antimicrobial resistance, where inappropriate usage leading to resistance may reduce the efficacy of life-saving drugs.
Abstract.
Author URL.
White A, Bell SS, Lurz PWW, Boots M (2014). Conservation management within strongholds in the face of disease-mediated invasions: Red and grey squirrels as a case study.
Journal of Applied Ecology,
51(6), 1631-1642.
Abstract:
Conservation management within strongholds in the face of disease-mediated invasions: Red and grey squirrels as a case study
There is increasing evidence that disease-mediated invasions are widespread across a range of vertebrate, invertebrate and plant systems. We therefore need a better understanding of the role of disease in managing conservation threats due to introduced and invasive species. Here, we develop a general theoretical model framework to assess the impact of disease-mediated invasion on the viability of conserving native species through refuges taking into account explicit spatial and stochastic processes. The model techniques are applied to the well-documented red and grey squirrel conservation system in the UK as a case study. By combining general and specific modelling approaches, we are able to make management predictions while also gaining an understanding of the processes that underlie population outcomes leading to more robust conservation practice. Model results indicate that in the absence of control of the invading species, native populations are driven to extinction both in the absence of disease (through competition) and more rapidly when the disease is included (through competition and disease processes). When control is applied to reduce the abundance of the invading species, there is a threshold in the level of control, above which the invading population can be prevented from establishing and the native species can be protected. Highly virulent infections - squirrelpox in red squirrels - lead to periodic outbreaks of disease in the native population due to continual invasion attempts from the disease-carrying invader. Infections with low virulence may become established at endemic levels in native populations. Therefore, an important finding is that the disease can spread through the native species even when the invading species is prevented from establishing. The benefits of increased density may be countered by an increased risk of disease outbreaks. Therefore, a critical message is that there is a correlation between native density (and therefore habitat quality) and the impact of disease 'harmful' to native species. Control of the invading species to prevent it establishing in strongholds can protect the native species from exclusion, but may not protect it from disease outbreaks. Synthesis and applications. Disease outbreaks in the absence of the invading species can result in significant population crashes and therefore represents a serious threat because it contributes to the risk of population extinction by suppressing the size of the population making it more vulnerable to extinction through stochastic processes. Disease outbreaks in the absence of the invading species can result in significant population crashes and therefore represents a serious threat because it contributes to the risk of population extinction by suppressing the size of the population making it more vulnerable to extinction through stochastic processes.
Abstract.
White A, Bell SS, Lurz PWW, Boots M (2014). Conservation management within strongholds in the face of disease-mediated invasions: Red and grey squirrels as a case study. Journal of Applied Ecology
Ryder JJ, Hoare M-J, Pastok D, Bottery M, Boots M, Fenton A, Atkinson D, Knell RJ, Hurst GDD (2014). Disease epidemiology in arthropods is altered by the presence of nonprotective symbionts.
Am Nat,
183(3), E89-104.
Abstract:
Disease epidemiology in arthropods is altered by the presence of nonprotective symbionts.
Inherited microbial symbionts can modulate host susceptibility to natural enemy attack. A wider range of symbionts influence host population demography without altering individual susceptibility, and it has been suggested that these may modify host disease risk through altering the rate of exposure to natural enemies. We present the first test of this thesis, specifically testing whether male-killing symbionts alter the epidemiology of a sexually transmitted infection (STI) carried by its host. STIs are typically expected to show female-biased epidemics, and we first present a simple model which indicates that male-biased STI epidemics may occur where symbionts create female-biased population sex ratios. We then examined the dynamics of a STI in the ladybird beetle Adalia bipunctata, which is also host to a male-killing bacterium. We present evidence that male-biased epidemics of the STI are observed in natural populations when the male-killer is common. Laboratory experiments did not support a role for differential susceptibility of male and female hosts to the STI, nor a protective role for the symbiont, in creating this bias. We conclude that the range of symbionts likely to alter parasite epidemiology will be much wider than previously envisaged, because it will additionally include those that impact host demography alone.
Abstract.
Author URL.
Lopez Pascua L, Hall AR, Best A, Morgan AD, Boots M, Buckling A (2014). Higher resources decrease fluctuating selection during host-parasite coevolution.
Ecology Letters,
17(11), 1380-1388.
Abstract:
Higher resources decrease fluctuating selection during host-parasite coevolution
We still know very little about how the environment influences coevolutionary dynamics. Here, we investigated both theoretically and empirically how nutrient availability affects the relative extent of escalation of resistance and infectivity (arms race dynamic; ARD) and fluctuating selection (fluctuating selection dynamic; FSD) in experimentally coevolving populations of bacteria and viruses. By comparing interactions between clones of bacteria and viruses both within- and between-time points, we show that increasing nutrient availability resulted in coevolution shifting from FSD, with fluctuations in average infectivity and resistance ranges over time, to ARD. Our model shows that range fluctuations with lower nutrient availability can be explained both by elevated costs of resistance (a direct effect of nutrient availability), and reduced benefits of resistance when population sizes of hosts and parasites are lower (an indirect effect). Nutrient availability can therefore predictably and generally affect qualitative coevolutionary dynamics by both direct and indirect (mediated through ecological feedbacks) effects on costs of resistance.
Abstract.
Lopez Pascua L, Hall AR, Best A, Morgan AD, Boots M, Buckling A (2014). Higher resources decrease fluctuating selection during host-parasite coevolution.
Ecol Lett,
17(11), 1380-1388.
Abstract:
Higher resources decrease fluctuating selection during host-parasite coevolution.
We still know very little about how the environment influences coevolutionary dynamics. Here, we investigated both theoretically and empirically how nutrient availability affects the relative extent of escalation of resistance and infectivity (arms race dynamic; ARD) and fluctuating selection (fluctuating selection dynamic; FSD) in experimentally coevolving populations of bacteria and viruses. By comparing interactions between clones of bacteria and viruses both within- and between-time points, we show that increasing nutrient availability resulted in coevolution shifting from FSD, with fluctuations in average infectivity and resistance ranges over time, to ARD. Our model shows that range fluctuations with lower nutrient availability can be explained both by elevated costs of resistance (a direct effect of nutrient availability), and reduced benefits of resistance when population sizes of hosts and parasites are lower (an indirect effect). Nutrient availability can therefore predictably and generally affect qualitative coevolutionary dynamics by both direct and indirect (mediated through ecological feedbacks) effects on costs of resistance.
Abstract.
Author URL.
Boots M, White A, Best A, Bowers R (2014). How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites.
Evolution,
68(6), 1594-1606.
Abstract:
How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites
There is typically considerable variation in the level of infectivity of parasites and the degree of resistance of hosts within populations. This trait variation is critical not only to the evolutionary dynamics but also to the epidemiology, and potentially the control of infectious disease. However, we lack an understanding of the processes that generate and maintain this trait diversity. We examine theoretically how epidemiological feedbacks and the characteristics of the interaction between host types and parasites strains determine the coevolution of host-parasite diversity. The interactions include continuous characterizations of the key phenotypic features of classic gene-for-gene and matching allele models. We show that when there are costs to resistance in the hosts and infectivity in the parasite, epidemiological feedbacks may generate diversity but this is limited to dimorphism, often of extreme types, in a broad range of realistic infection scenarios. For trait polymorphism, there needs to be both specificity of infection between host types and parasite strains as well as incompatibility between particular strains and types. We emphasize that although the high specificity is well known to promote temporal "Red Queen" diversity, it is costs and combinations of hosts and parasites that cannot infect that will promote static trait diversity. © 2014 the Authors. Evolution published by Wiley Periodicals, Inc. on behalf of the Society for the Study of Evolution.
Abstract.
Boots M, White A, Best A, Bowers R (2014). How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites.
Evolution,
68(6), 1594-1606.
Abstract:
How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites.
There is typically considerable variation in the level of infectivity of parasites and the degree of resistance of hosts within populations. This trait variation is critical not only to the evolutionary dynamics but also to the epidemiology, and potentially the control of infectious disease. However, we lack an understanding of the processes that generate and maintain this trait diversity. We examine theoretically how epidemiological feedbacks and the characteristics of the interaction between host types and parasites strains determine the coevolution of host-parasite diversity. The interactions include continuous characterizations of the key phenotypic features of classic gene-for-gene and matching allele models. We show that when there are costs to resistance in the hosts and infectivity in the parasite, epidemiological feedbacks may generate diversity but this is limited to dimorphism, often of extreme types, in a broad range of realistic infection scenarios. For trait polymorphism, there needs to be both specificity of infection between host types and parasite strains as well as incompatibility between particular strains and types. We emphasize that although the high specificity is well known to promote temporal "Red Queen" diversity, it is costs and combinations of hosts and parasites that cannot infect that will promote static trait diversity.
Abstract.
Author URL.
Best A, White A, Boots M (2014). The coevolutionary implications of host tolerance.
Evolution,
68(5), 1426-1435.
Abstract:
The coevolutionary implications of host tolerance.
Host tolerance to infectious disease, whereby hosts do not directly "fight" parasites but instead ameliorate the damage caused, is an important defense mechanism in both plants and animals. Because tolerance to parasite virulence may lead to higher prevalence of disease in a population, evolutionary theory tells us that while the spread of resistance genes will result in negative frequency dependence and the potential for diversification, the evolution of tolerance is instead likely to result in fixation. However, our understanding of the broader implications of tolerance is limited by a lack of fully coevolutionary theory. Here we examine the coevolution of tolerance across a comprehensive range of classic coevolutionary host-parasite frameworks, including equivalents of gene-for-gene and matching allele and evolutionary invasion models. Our models show that the coevolution of host tolerance and parasite virulence does not lead to the generation and maintenance of diversity through either static polymorphisms or through "Red-queen" cycles. Coevolution of tolerance may however lead to multiple stable states leading to sudden shifts in parasite impacts on host health. More broadly, we emphasize that tolerance may change host-parasite interactions from antagonistic to a form of "apparent commensalism," but may also lead to the evolution of parasites that are highly virulent in nontolerant hosts.
Abstract.
Author URL.
Wilson K, Coulson T, Boots M, Baker L, Livermore P (2014). The times they are a-changin': Evolution and revolution in animal ecology publishing. Journal of Animal Ecology, 83(1), 1-4.
2013
Rasheed SB, Butlin RK, Boots M (2013). A review of dengue as an emerging disease in Pakistan.
Public Health,
127(1), 11-17.
Abstract:
A review of dengue as an emerging disease in Pakistan
The presence of dengue virus has been detected using neutralization and haemagglutination inhibition antibodies in local populations in Pakistan since the 1960s. However, the first epidemic was not reported until 1994. This was followed by some cases in 1995, but the disease was confined to the port city of Karachi. Since 2006, dengue epidemics have occurred every year and the range has extended to most cities in Pakistan. Dengue now affects thousands of people and has caused hundreds of deaths. It has become a major health problem in Pakistan, and it is likely to become an even greater health problem in the coming years. This review gives an insight into the dengue situation from the early 1960s to the most recent epidemics in Pakistan, and also describes the primary vector of this disease (Aedes aegypti) in Pakistan. As such, it provides the first comprehensive review of the emergence of this important public health problem. © 2012 the Royal Institute of Public Health.
Abstract.
Webb SD, Keeling MJ, Boots M (2013). A theoretical study of the role of spatial population structure in the evolution of parasite virulence.
Theor Popul Biol,
84, 36-45.
Abstract:
A theoretical study of the role of spatial population structure in the evolution of parasite virulence.
The rich theory of infectious disease modelling using the Susceptible-Infectious-Recovered (SIR) framework is mainly based on the assumption of a well-mixed population, under which evolutionary behaviours (typically derived using adaptive dynamics) are shown to depend critically on the qualitative features of a virulence-transmission trade-off. Spatial extensions of this work, using simulation studies, show multiple evolutionary outcomes, which strongly depend on trade-off shape and, additionally, the length scale of the infectious process. In this paper, we aim to shed analytical insight into the mechanisms underlying these spatial evolutionary outcomes. In particular, why there is a qualitative difference observed in the evolutionary predicted virulence rates between linear and decelerating trade-offs between transmission and virulence and how recovery can weaken the effect of space. We use both pair approximations and cellular automata to model the spatial populations and the analysis exploits small neighbourhood variations in the spatial settings. The evolutionary outcomes are derived using adaptive dynamics.
Abstract.
Author URL.
Leggett HC, Buckling A, Long GH, Boots M (2013). Generalism and the evolution of parasite virulence.
Trends in Ecology and Evolution,
28(10), 592-596.
Abstract:
Generalism and the evolution of parasite virulence
The evolution of parasite-imposed host harm (virulence) will be affected by numerous factors, not least the range of hosts that parasites can infect. Here, we consider four ways that parasite host range (generalism) might directly affect observed levels of parasite virulence: costs of generalism, multiplicity of infection, maladaptive virulence, and host availability. Integrating parasite infectivity range with life-history evolution will generate novel general hypotheses for the evolutionary ecology of virulence, as well as explicit predictions about the virulence of emerging diseases resulting from host shifts. © 2013 Elsevier Ltd.
Abstract.
Leggett HC, Buckling A, Long GH, Boots M (2013). Generalism and the evolution of parasite virulence.
Trends Ecol Evol,
28(10), 592-596.
Abstract:
Generalism and the evolution of parasite virulence.
The evolution of parasite-imposed host harm (virulence) will be affected by numerous factors, not least the range of hosts that parasites can infect. Here, we consider four ways that parasite host range (generalism) might directly affect observed levels of parasite virulence: costs of generalism, multiplicity of infection, maladaptive virulence, and host availability. Integrating parasite infectivity range with life-history evolution will generate novel general hypotheses for the evolutionary ecology of virulence, as well as explicit predictions about the virulence of emerging diseases resulting from host shifts.
Abstract.
Author URL.
Boots M, Donnelly R, White A (2013). Optimal immune defence in the light of variation in lifespan.
Parasite Immunol,
35(11), 331-338.
Abstract:
Optimal immune defence in the light of variation in lifespan.
There is good evidence for costs to both the uses of immune defences and their development and maintenance. The optimal defence will be a balance of these costs with the risk of infection and the virulence of the disease. It is therefore clear that the life-history characteristics of both host and parasite will impact the optimal level of defence, and that this may in part explain the variation in immune defence against different pathogens and parasites. For instance, it has traditionally been suggested that long-lived hosts should invest in immune memory. Ecological evolutionary theory can be used to examine in detail how different host characteristics will affect the optimal immune response that evolves. Here, we review theoretical studies on the impact of host lifespan on various immune defence characteristics including acquired immunity and highlight the importance of population-level epidemiological feedbacks on the outcome. In particular, we discuss when longer-lived hosts may invest less in acquired immunity and develop new theory to highlight the importance of the mechanism of host population regulation to the outcome. We finish by discussing where more theory is needed and how comparative and experimental studies may test the theory.
Abstract.
Author URL.
Rasheed SB, Boots M, Frantz AC, Butlin RK (2013). Population structure of the mosquito Aedes aegypti (Stegomyia aegypti) in Pakistan.
Med Vet Entomol,
27(4), 430-440.
Abstract:
Population structure of the mosquito Aedes aegypti (Stegomyia aegypti) in Pakistan.
Eleven microsatellite markers were used to determine the genetic population structure and spread of Aedes aegypti (Stegomyia aegypti) (Diptera: Culicidae) in Pakistan using mosquitoes collected from 13 different cities. There is a single genetic cluster of Ae. aegypti in Pakistan with a pattern of isolation by distance within the population. The low level of isolation by distance suggests the long-range passive dispersal of this mosquito, which may be facilitated by the tyre trade in Pakistan. A decrease in genetic diversity from south to north suggests a recent spread of this mosquito from Karachi. A strong negative correlation between genetic distance and the quality of road connections shows that populations in cities connected by better road networks are less differentiated, which suggests the human-aided passive dispersal of Ae. aegypti in Pakistan. Dispersal on a large spatial scale may facilitate the strategy of introducing transgenic Ae. aegypti or intracellular bacteria such as Wolbachia to control the spread of dengue disease in Pakistan, but it also emphasizes the need for simple measures to control container breeding sites.
Abstract.
Author URL.
Coulson T, Hays G, Boots M, Wilson K, Baker L, Livermore P (2013). Publishing the best original research in animal ecology: Looking forward from 2013. Journal of Animal Ecology, 82(1), 1-2.
Donnelly R, Best A, White A, Boots M (2013). Seasonality selects for more acutely virulent parasites when virulence is density dependent.
Proc Biol Sci,
280(1751).
Abstract:
Seasonality selects for more acutely virulent parasites when virulence is density dependent.
Host condition is often likely to influence parasite virulence. Furthermore, condition may often be correlated with host density, and therefore, it is important to understand the role of density-dependent virulence (DDV). We examine the consequences of DDV to the evolution of parasites in both seasonal and non-seasonal environments. In particular, we consider seasonality in host birth rate that results in a fluctuating host density and therefore a variable virulence. We show that parasites are selected for lower exploitation, and therefore lower transmission and virulence as the strength of DDV increases without seasonality. This is an important insight from our models; DDV has the opposite effect on the evolution of parasites to that of higher baseline mortality. Our key result is that although seasonality does not affect the evolution of virulence in classical models, with DDV parasites in seasonal environments are predicted to evolve to be more acute. This suggests that in more seasonal environments wildlife disease is likely to be more rather than less virulent if DDV is widespread.
Abstract.
Author URL.
Ryder JJ, Pastok D, Hoare MJ, Bottery MJ, Boots M, Knell RK, Atkinson D, Hurst GDD (2013). Spatial variation in food supply, mating behavior, and sexually transmitted disease epidemics.
Behavioral Ecology,
24(3), 723-729.
Abstract:
Spatial variation in food supply, mating behavior, and sexually transmitted disease epidemics
Mating behavior helps to shape the epidemiology of sexually transmitted infections (STIs) by determining the rate at which infectious and susceptible individuals make contact. To the extent that mating behavior shows spatial variation, it is expected that STI epidemics will also show spatial heterogeneity (provided that dispersal is limited). However, empirical data are lacking for natural systems. Here, therefore, we investigate the association between local mating behavior and STI epidemiology in natural populations of the two-spot ladybird, Adalia bipunctata, and dissect the causes of this variation. Variation in mating behavior was observed over local and regional spatial scales and high mating rate led to stronger local epidemics of the STI. Initial ecological observations suggested that reduced mating rate was associated largely with low food supply (and possibly to a lesser extent with local population density) and not with differences in thermal environment. We tested the potential role of food supply in fuelling STI epidemics in laboratory populations and confirmed that high food provision led to greater STI transmission. We conclude that food supply is strongly associated with mating rate in the field and that this produces heterogeneity in STI epidemiology. A consequence is that STI-induced sterility will reduce reproduction in habitat patches of high food quality. © 2012 the Author.
Abstract.
Best A, Tidbury H, White A, Boots M (2013). The evolutionary dynamics of within-generation immune priming in invertebrate hosts.
Journal of the Royal Society Interface,
10(80).
Abstract:
The evolutionary dynamics of within-generation immune priming in invertebrate hosts
While invertebrates lack the machinery necessary for 'acquired immunity', there is increasing empirical evidence that exposure to low levels of disease may 'prime' an invertebrate's immune response, increasing its defence to subsequent exposure. Despite this increasing empirical data, there has been little theoretical attention paid to immune priming. Here, we investigate the evolution of immune priming, focusing on the role of the unique feedbacks generated by a newly developed susceptible-primed-infected epidemiological model. Contrasting our results with previous models on the evolution of acquired immunity, we highlight that there are important implications to the evolution of immunity through priming owing to these different epidemiological feedbacks. In particular, we find that in contrast to acquired immunity, priming is strongly selected for at high as well as intermediate pathogen virulence. We also find that priming may be greatest at either intermediate or high host lifespans depending on the severity of disease. Furthermore, hosts faced with more severe pathogens are more likely to evolve diversity in priming. Finally, we show when the evolution of priming leads to the exclusion of the pathogens or hosts experiencing population cycles. Overall the model acts as a baseline for understanding the evolution of priming in host-pathogen systems. © 2013 the Authors.
Abstract.
Best A, Tidbury H, White A, Boots M (2013). The evolutionary dynamics of within-generation immune priming in invertebrate hosts.
J R Soc Interface,
10(80).
Abstract:
The evolutionary dynamics of within-generation immune priming in invertebrate hosts.
While invertebrates lack the machinery necessary for 'acquired immunity', there is increasing empirical evidence that exposure to low levels of disease may 'prime' an invertebrate's immune response, increasing its defence to subsequent exposure. Despite this increasing empirical data, there has been little theoretical attention paid to immune priming. Here, we investigate the evolution of immune priming, focusing on the role of the unique feedbacks generated by a newly developed susceptible-primed-infected epidemiological model. Contrasting our results with previous models on the evolution of acquired immunity, we highlight that there are important implications to the evolution of immunity through priming owing to these different epidemiological feedbacks. In particular, we find that in contrast to acquired immunity, priming is strongly selected for at high as well as intermediate pathogen virulence. We also find that priming may be greatest at either intermediate or high host lifespans depending on the severity of disease. Furthermore, hosts faced with more severe pathogens are more likely to evolve diversity in priming. Finally, we show when the evolution of priming leads to the exclusion of the pathogens or hosts experiencing population cycles. Overall the model acts as a baseline for understanding the evolution of priming in host-pathogen systems.
Abstract.
Author URL.
Antonovics J, Boots M, Ebert D, Koskella B, Poss M, Sadd BM (2013). The origin of specificity by means of natural selection: Evolved and nonhost resistance in host-pathogen interactions.
Evolution,
67(1), 1-9.
Abstract:
The origin of specificity by means of natural selection: Evolved and nonhost resistance in host-pathogen interactions
Most species seem to be completely resistant to most pathogens and parasites. This resistance has been called "nonhost resistance" because it is exhibited by species that are considered not to be part of the normal host range of the pathogen. A conceptual model is presented suggesting that failure of infection on nonhosts may be an incidental by-product of pathogen evolution leading to specialization on their source hosts. This model is contrasted with resistance that results from hosts evolving to resist challenge by their pathogens, either as a result of coevolution with a persistent pathogen or as the result of one-sided evolution by the host against pathogens that are not self-sustaining on those hosts. Distinguishing evolved from nonevolved resistance leads to contrasting predictions regarding the relationship between resistance and genetic distance. An analysis of cross-inoculation experiments suggests that the resistance is often the product of pathogen specialization. Understanding the contrasting evolutionary origins of resistance is critical for studies on the genetics and evolution of host-pathogen interactions in human, agricultural, and natural populations. Research on human infectious disease using animal models may often study resistances that have quite contrasting evolutionary origins, and therefore very different underlying genetic mechanisms. © 2012 the Author(s). Evolution © 2012 the Society for the Study of Evolution.
Abstract.
Webb SD, Keeling MJ, Boots M (2013). The role of spatial population structure on the evolution of parasites with acquired immunity and demography.
J Theor Biol,
324, 21-31.
Abstract:
The role of spatial population structure on the evolution of parasites with acquired immunity and demography.
It is clear that the evolution of infectious disease may be influenced by population spatial structure and transmission networks but we lack an understanding of the role of acquired immunity. Here we examine theoretically the role of spatial structure in the evolution of infectious disease described by the classic Susceptible, Infected, Recovered (SIR) model focusing on the impact of host demographics. We find that, for the classic assumption of a trade-off between transmission and virulence, localised transmission does favor, as predicted from other models, chronic pathogens with low transmission and virulence, but that this effect reduces as the recovery rate increases. However, under the assumption that pathogens reproduce rapidly within the host are harder to clear but result in higher virulence local interactions favor more virulent parasites and, depending on the nature of the disease interaction, can increase or decrease the chance of evolutionary bistabilities that may lead to sudden persistent changes in virulence. Therefore, our work further emphasizes the importance of spatial structure to parasite evolution. This spatial evolutionary theory is important because it predicts how different pathogens may respond to changes in patterns of mixing.
Abstract.
Author URL.
2012
Prajsnar TK, Hamilton R, Garcia-Lara J, McVicker G, Williams A, Boots M, Foster SJ, Renshaw SA (2012). A privileged intraphagocyte niche is responsible for disseminated infection of Staphylococcus aureus in a zebrafish model.
Cell Microbiol,
14(10), 1600-1619.
Abstract:
A privileged intraphagocyte niche is responsible for disseminated infection of Staphylococcus aureus in a zebrafish model.
The innate immune system is the primary defence against the versatile pathogen, Staphylococcus aureus. How this organism is able to avoid immune killing and cause infections is poorly understood. Using an established larval zebrafish infection model, we have shown that overwhelming infection is due to subversion of phagocytes by staphylococci, allowing bacteria to evade killing and found foci of disease. Larval zebrafish coinfected with two S. aureus strains carrying different fluorescent reporter gene fusions (but otherwise isogenic) had bacterial lesions, at the time of host death, containing predominantly one strain. Quantitative data using two marked strains revealed that the strain ratios, during overwhelming infection, were often skewed towards the extremes, with one strain predominating. Infection with passaged bacterial clones revealed the phenomenon not to bedue to adventitious mutations acquired by the pathogen. After infection of the host, all bacteria are internalized by phagocytes and the skewing of population ratios is absolutely dependent on the presence of phagocytes. Mathematical modelling of pathogen population dynamics revealed the data patterns are consistent with the hypothesis that a small number of infected phagocytes serve as an intracellular reservoir for S. aureus, which upon release leads to disseminated infection. Strategies to specifically alter neutrophil/macrophage numbers were used to map the potential subpopulation of phagocytes acting as a pathogen reservoir, revealing neutrophils as the likely 'niche'. Subsequently in a murine sepsis model, S. aureus abscesses in kidneys were also found to be predominantly clonal, therefore likely founded by an individual cell, suggesting a potential mechanism analogous to the zebrafish model with few protected niches. These findings add credence to the argument that S. aureus control regimes should recognize both the intracellular as well as extracellular facets of the S. aureus life cycle.
Abstract.
Author URL.
Prajsnar TK, Hamilton R, Garcia-Lara J, Mcvicker G, Williams A, Boots M, Foster SJ, Renshaw SA (2012). A privileged intraphagocyte niche is responsible for disseminated infection of staphylococcus aureus in a zebrafish model.
Cellular Microbiology,
14(10), 1600-1619.
Abstract:
A privileged intraphagocyte niche is responsible for disseminated infection of staphylococcus aureus in a zebrafish model
The innate immune system is the primary defence against the versatile pathogen, Staphylococcus aureus. How this organism is able to avoid immune killing and cause infections is poorly understood. Using an established larval zebrafish infection model, we have shown that overwhelming infection is due to subversion of phagocytes by staphylococci, allowing bacteria to evade killing and found foci of disease. Larval zebrafish coinfected with two S.aureus strains carrying different fluorescent reporter gene fusions (but otherwise isogenic) had bacterial lesions, at the time of host death, containing predominantly one strain. Quantitative data using two marked strains revealed that the strain ratios, during overwhelming infection, were often skewed towards the extremes, with one strain predominating. Infection with passaged bacterial clones revealed the phenomenon not to bedue to adventitious mutations acquired by the pathogen. After infection of the host, all bacteria are internalized by phagocytes and the skewing of population ratios is absolutely dependent on the presence of phagocytes. Mathematical modelling of pathogen population dynamics revealed the data patterns are consistent with the hypothesis that a small number of infected phagocytes serve as an intracellular reservoir for S.aureus, which upon release leads to disseminated infection. Strategies to specifically alter neutrophil/macrophage numbers were used to map the potential subpopulation of phagocytes acting as a pathogen reservoir, revealing neutrophils as the likely 'niche'. Subsequently in a murine sepsis model, S.aureus abscesses in kidneys were also found to be predominantly clonal, therefore likely founded by an individual cell, suggesting a potential mechanism analogous to the zebrafish model with few protected niches. These findings add credence to the argument that S.aureus control regimes should recognize both the intracellular as well as extracellular facets of the S.aureus life cycle. © 2012 Blackwell Publishing Ltd.
Abstract.
Rasheed SB, Butlin RK, Boots M (2012). A review of dengue as an emerging disease in Pakistan. Public Health
Strauss A, White A, Boots M (2012). Invading with biological weapons: the importance of disease-mediated invasions.
Functional Ecology,
26(6), 1249-1261.
Abstract:
Invading with biological weapons: the importance of disease-mediated invasions
Invasive organisms and emerging wildlife disease pose two of the greatest threats to global biodiversity and ecosystem functioning. Typically, when parasites are considered in invasion biology, it is in the context of the enemy release hypothesis, wherein a non-indigenous species has greater probability of invasion success by virtue of leaving its natural enemies, including parasites, behind. It is also possible that native parasites may prevent invasions, but it is clear that invasive organisms may bring infectious diseases with them that can infect native competitors (via spillover), or act as competent hosts for native diseases, increasing disease prevalence among native species (via spillback). If the shared disease (either via spillover or spillback) has higher virulence in the native host (which is particularly likely with introduced parasites), there is the potential that the disease can act as a 'biological weapon' leading to a disease-mediated invasion (DMI). Here, we review cases where disease may have been an important factor mediating a wide range of invasions in vertebrates, invertebrates and plants. We then focus on the invasion of the grey squirrel into the UK as a case study of a DMI, and we discuss how mathematical models have helped us to understand the importance of this shared disease and its implications for the management of invasive species. We conclude that (i) DMIs are a widespread phenomenon, that (ii) spillover is more common in animal invasions and spillback more common among plant invasions and that (iii) spillover DMIs are particularly important in explaining the replacement of native animals with phylogenetically similar non-indigenous species. © 2012 British Ecological Society.
Abstract.
Best A, Webb S, Antonovics J, Boots M (2012). Local transmission processes and disease-driven host extinctions.
Theoretical Ecology,
5(2), 211-217.
Abstract:
Local transmission processes and disease-driven host extinctions
Classic infectious disease theory assumes that transmission depends on either the global density of the parasite (for directly transmitted diseases) or its global frequency (for sexually transmitted diseases). One important implication of this dichotomy is that parasite-driven host extinction is only predicted under frequency-dependent transmission. However, transmission is fundamentally a local process between individuals that is determined by their and/or their vector's behaviour. We examine the implications of local transmission processes to the likelihood of disease-driven host extinction. Local density-dependent transmission can lead to parasite-driven extinction, but extinction is more likely under local frequency-dependent transmission and much more likely when there is active local searching behaviour. Density-dependent directly transmitted diseases spread locally can therefore lead to deterministic host extinction, but locally frequency-dependent passive vector-borne diseases are more likely to cause extinctions. However, it is active searching behaviour either by a vector or between sexual partners that is most likely to cause the host to go extinct. Our work emphasises that local processes are essential in determining parasite-driven extinctions, and the role of parasites in the extinction of rare species may have been underplayed due to the classic assumption of global density-dependent transmission. © 2011 Springer Science+Business Media B.V.
Abstract.
Boots M, Roberts KE (2012). Maternal effects in disease resistance: poor maternal environment increases offspring resistance to an insect virus.
Proc Biol Sci,
279(1744), 4009-4014.
Abstract:
Maternal effects in disease resistance: poor maternal environment increases offspring resistance to an insect virus.
Maternal effects can be adaptive and because of their intrinsic time delays may have important effects on population dynamics. In vertebrates, and increasingly invertebrates, it is well established that offspring defence is in part determined by maternal parasite exposure. It has also been suggested that there may be indirect maternal effects on immunity mediated by other components of the maternal environment, including density and resource availability. Here, we examine the effect maternal resource availability has on the immunity of offspring in an insect-virus system. We use five different maternal resource levels and examine immunity in the offspring both directly, by challenge with a virus, and by measuring a major component of the immune system, across three offspring environments. Both the direct infection assay and the measure of immunocompetence show clearly that offspring from mothers in poor environments are more resistant to parasites. This may result from life-history optimization of mothers in poor environments, or because the poor environment acts as a cue for higher disease risk in the next generation. This emphasizes the importance of maternal effects on disease resistance, mediated through indirect environmental factors that will have important implications to both the ecological and evolutionary dynamics of host-parasite interactions.
Abstract.
Author URL.
Dieng H, Rahman GMS, Hassan AA, Salmah MRC, Satho T, Miake F, Boots M, Sazaly AB (2012). The effects of simulated rainfall on immature population dynamics of Aedes albopictus and female oviposition.
International Journal of Biometeorology,
56(1), 113-120.
Abstract:
The effects of simulated rainfall on immature population dynamics of Aedes albopictus and female oviposition
Larvae of Aedes albopictus Skuse typically inhabit natural and artificial containers. Since these larval habitats are replenished by rainfall, Ae. albopictus may experience increased loss of immature stages in areas with high levels of rainfall. In this study, we investigated the effects of rainfall and container water level on population density, and oviposition activity of Ae. albopictus. In field and laboratory experiments, we found that rainfall resulted in the flushing of breeding habitats. Excess rain negatively impacted larval and pupal retention, especially in small habitats. When filled with water to overflowing, container habitats were significantly repellent to ovipositing females. Taken together, these data suggest that rainfall triggers population loss of Ae. albopictus and related species through a direct detrimental effect (flushing out) and an indirect effect (ovipositional repellency). © 2011 ISB.
Abstract.
Tidbury HJ, Best A, Boots M (2012). The epidemiological consequences of immune priming.
Proc Biol Sci,
279(1746), 4505-4512.
Abstract:
The epidemiological consequences of immune priming.
Exposure to low doses of pathogens that do not result in the host becoming infectious may 'prime' the immune response and increase protection to subsequent challenge. There is increasing evidence that such immune priming is a widespread and important feature of invertebrate host-pathogen interactions. Immune priming clearly has implications for individual hosts but will also have population-level implications. We present a susceptible-primed-infectious model-in contrast to the classic susceptible-infectious-recovered framework-to investigate the impacts of immune priming on pathogen persistence and population stability. We describe impacts of immune priming on the epidemiology of the disease in both constant and seasonal environments. A key result is that immune priming may act to destabilize population dynamics. In particular, when the proportion of individuals becoming primed rather than infected is high, but this priming does not confer full immunity, the population may be strongly destabilized through the generation of limit cycles. We discuss the implications of our model both in the context of invertebrate immunity and more widely.
Abstract.
Author URL.
Best A, Long G, White A, Boots M (2012). The implications of immunopathology for parasite evolution.
Proc Biol Sci,
279(1741), 3234-3240.
Abstract:
The implications of immunopathology for parasite evolution.
By definition, parasites harm their hosts, but in many infections much of the pathology is driven by the host immune response rather than through direct damage inflicted by parasites. While these immunopathological effects are often well studied and understood mechanistically in individual disease interactions, there remains relatively little understanding of their broader impact on the evolution of parasites and their hosts. Here, we theoretically investigate the implications of immunopathology, broadly defined as additional mortality associated with the host's immune response, on parasite evolution. In particular, we examine how immunopathology acting on different epidemiological traits (namely transmission, virulence and recovery) affects the evolution of disease severity. When immunopathology is costly to parasites, such that it reduces their fitness, for example by decreasing transmission, there is always selection for increased disease severity. However, we highlight a number of host-parasite interactions where the parasite may benefit from immunopathology, and highlight scenarios that may lead to the evolution of slower growing parasites and potentially reduced disease severity. Importantly, we find that conclusions on disease severity are highly dependent on how severity is measured. Finally, we discuss the effect of treatments used to combat disease symptoms caused by immunopathology.
Abstract.
Author URL.
Boots M, White A, Best A, Bowers R (2012). The importance of who infects whom: the evolution of diversity in host resistance to infectious disease.
Ecology Letters,
15(10), 1104-1111.
Abstract:
The importance of who infects whom: the evolution of diversity in host resistance to infectious disease
Variation for resistance to infectious disease is ubiquitous and critical to host and parasite evolution and to disease impact, spread and control. However, the processes that generate and maintain this diversity are not understood. We examine how ecological feedbacks generate diversity in host defence focussing on when polymorphism can evolve without co-evolution of the parasite. Our key result is that when there is heritable variation in hosts in both their transmissibility and susceptibility along with costs to resistance, there is the possibility of the evolution of polymorphism. We argue that a wide range of behavioural or physiological mechanisms may lead to relationships between transmissibility and susceptibility that generate diversity. We illustrate this by showing that a tendency for higher contacts between related individuals leads to polymorphism. Only dimorphisms can evolve when infection is determined only by an individuals' susceptibility or when transmissibility and susceptibility are simply positively or negatively correlated. © 2012 Blackwell Publishing Ltd/CNRS.
Abstract.
Boots M, White A, Best A, Bowers R (2012). The importance of who infects whom: the evolution of diversity in host resistance to infectious disease.
Ecology Letters,
15(10), 1104-1111.
Abstract:
The importance of who infects whom: the evolution of diversity in host resistance to infectious disease
Variation for resistance to infectious disease is ubiquitous and critical to host and parasite evolution and to disease impact, spread and control. However, the processes that generate and maintain this diversity are not understood. We examine how ecological feedbacks generate diversity in host defence focussing on when polymorphism can evolve without co-evolution of the parasite. Our key result is that when there is heritable variation in hosts in both their transmissibility and susceptibility along with costs to resistance, there is the possibility of the evolution of polymorphism. We argue that a wide range of behavioural or physiological mechanisms may lead to relationships between transmissibility and susceptibility that generate diversity. We illustrate this by showing that a tendency for higher contacts between related individuals leads to polymorphism. Only dimorphisms can evolve when infection is determined only by an individuals' susceptibility or when transmissibility and susceptibility are simply positively or negatively correlated. © 2012 Blackwell Publishing Ltd/CNRS.
Abstract.
Boots M, White A, Best A, Bowers R (2012). The importance of who infects whom: the evolution of diversity in host resistance to infectious disease.
Ecol Lett,
15(10), 1104-1111.
Abstract:
The importance of who infects whom: the evolution of diversity in host resistance to infectious disease.
Variation for resistance to infectious disease is ubiquitous and critical to host and parasite evolution and to disease impact, spread and control. However, the processes that generate and maintain this diversity are not understood. We examine how ecological feedbacks generate diversity in host defence focussing on when polymorphism can evolve without co-evolution of the parasite. Our key result is that when there is heritable variation in hosts in both their transmissibility and susceptibility along with costs to resistance, there is the possibility of the evolution of polymorphism. We argue that a wide range of behavioural or physiological mechanisms may lead to relationships between transmissibility and susceptibility that generate diversity. We illustrate this by showing that a tendency for higher contacts between related individuals leads to polymorphism. Only dimorphisms can evolve when infection is determined only by an individuals' susceptibility or when transmissibility and susceptibility are simply positively or negatively correlated.
Abstract.
Author URL.
Antonovics J, Boots M, Ebert D, Koskella B, Poss M, Sadd BM (2012). The origin of specificity by means of natural selection: Evolved and nonhost resistance in host-pathogen interactions. Evolution
2011
Antonovics J, Boots M, Abbate J, Baker C, McFrederick Q, Panjeti V (2011). Biology and evolution of sexual transmission.
Abstract:
Biology and evolution of sexual transmission
Abstract.
Ahmad A, Ahmad AH, Dieng H, Satho T, Ahmad H, Aziz AT, Boots M (2011). Cadaver wrapping and arrival performance of adult flies in an oil palm plantation in northern Peninsular Malaysia.
Journal of Medical Entomology,
48(6), 1236-1246.
Abstract:
Cadaver wrapping and arrival performance of adult flies in an oil palm plantation in northern Peninsular Malaysia
There is accumulating evidence that criminals wrap dead bodies in an attempt to conceal evidence. To anticipate the forensic implications of this phenomenon, we examined whether flies that are naturally associated with cadavers exhibit a delay in attendance or differ in species composition and abundance patterns because of the presence of wrapping material. Wrapped and exposed carcasses of dead monkeys placed in an oil plantation in Kedah, Malaysia, were visited over 50 d. On daily visits to each of the six carcasses, visiting adult flies were sampled using hand nets. Flies of 12 families were encountered. Calliphoridae (Chrysomya rufifacies Macquart and C. megacephala (F.) was the most prevalent family, followed by Sphaeroceridae. Some families tended to be more abundant in WRCs (i.e. Calliphoridae, Muscidae, and Phoridae), whereas others (i.e. Piophilidae, Sepsidae, and Psychodidae) were more prevalent in exposed carcasses. Wrapping delayed the arrival of all fly species encountered, with delays varying from 1 to 13 d depending on species. Wrapping did not affect species composition of flies, but prolong the occurrence of some species. The results of the current study emphasize the need to take into consideration the presence of a wrap when estimating postmortem interval. © 2011 Entomological Society of America.
Abstract.
Dieng H, Saifur RGM, Ahmad AH, Md Rawi CS, Boots M, Satho T, Zuharah WF, Fadzly N, Althbyani A, Miake F, et al (2011). Discarded cigarette butts attract females and kill the progeny of aedes albopictus.
Journal of the American Mosquito Control Association,
27(3), 263-271.
Abstract:
Discarded cigarette butts attract females and kill the progeny of aedes albopictus
Discarded cigarette butts (DCB) waste occurs worldwide, pollutes landscapes, is unsightly, and results in added debris removal costs. There is, therefore, a great deal of current interest in making use of DCBs in beneficial ways. Despite evidence that DCBs are harmful to water fleas (Daphnia magna), which breed in aquatic environments as do mosquito larvae, their impact on dengue vectors is unknown. We examined whether Aedes albopictus alters its ovipositional responses, larval eclosion, and development in response to presence of DCBs in its habitats. We found oviposition activity in DCB-treated water similar to that of control water and that ovipositional activity in DCB solutions steadily increased over time as those solutions aged to 10 days. Larval eclosion was initially suppressed on day 1 in DCB solution, but increased thereafter to levels similar to control larval eclosion rates. The DCBwater solutions produced significantly higher mortality in both 1st and 2nd instars over control larvae for several days after initial exposure. Mortality rates decreased sharply 3 to 5 days postexposure as DCBs continued to decompose. We found increased survival rates during late development, but daily input of fresh DCBs prevented most young larvae from completing development. Taken together, these observations suggest that decomposing did not deter gravid Ae. albopictus females from ovipositing in treated containers and that DCB solutions had larvicidal effects on early instars. Our results are discussed in the context of DCB use to control container-breeding Ae. albopictus, a competent dengue vector in Asia and other parts of the world. © 2011 by the American Mosquito Control Association, Inc.
Abstract.
Vale PF, Wilson AJ, Best A, Boots M, Little TJ (2011). Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism.
American Naturalist,
177(4), 510-521.
Abstract:
Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism
Victims of infection are expected to suffer increasingly as parasite population growth increases. Yet, under some conditions, faster-growing parasites do not appear to cause more damage, and infections can be quite tolerable. We studied these conditions by assessing how the relationship between parasite population growth and host health is sensitive to environmental variation. In experimental infections of the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa, we show how easily an interaction can shift from a severe interaction, that is, when host fitness declines substantially with each unit of parasite growth, to a tolerable relationship by changing only simple environmental variables: temperature and food availability. We explored the evolutionary and epidemiological implications of such a shift by modeling pathogen evolution and disease spread under different levels of infection severity and found that environmental shifts that promote tolerance ultimately result in populations harboring more parasitized individuals. We also find that the opportunity for selection, as indicated by the variance around traits, varied considerably with the environmental treatment. Thus, our results suggest two mechanisms that could underlie coevolutionary hotspots and coldspots: spatial variation in tolerance and spatial variation in the opportunity for selection. © 2011 by the University of Chicago.
Abstract.
Best A, Webb S, White A, Boots M (2011). Host resistance and coevolution in spatially structured populations.
Proc Biol Sci,
278(1715), 2216-2222.
Abstract:
Host resistance and coevolution in spatially structured populations.
Natural, agricultural and human populations are structured, with a proportion of interactions occurring locally or within social groups rather than at random. This within-population spatial and social structure is important to the evolution of parasites but little attention has been paid to how spatial structure affects the evolution of host resistance, and as a consequence the coevolutionary outcome. We examine the evolution of resistance across a range of mixing patterns using an approximate mathematical model and stochastic simulations. As reproduction becomes increasingly local, hosts are always selected to increase resistance. More localized transmission also selects for higher resistance, but only if reproduction is also predominantly local. If the hosts disperse, lower resistance evolves as transmission becomes more local. These effects can be understood as a combination of genetic (kin) and ecological structuring on individual fitness. When hosts and parasites coevolve, local interactions select for hosts with high defence and parasites with low transmissibility and virulence. Crucially, this means that more population mixing may lead to the evolution of both fast-transmitting highly virulent parasites and reduced resistance in the host.
Abstract.
Author URL.
Long GH, Boots M (2011). How can immunopathology shape the evolution of parasite virulence?.
Trends Parasitol,
27(7), 300-305.
Abstract:
How can immunopathology shape the evolution of parasite virulence?
Immunopathology (immune-mediated pathology) is a ubiquitous cause of disease during infection, but how will parasite exploitation strategies evolve in its presence? Immunopathology can act to increase parasite fitness if it increases transmission rate, but can equally act to decrease parasite fitness if it increases host mortality. The focus here is on understanding how immunopathology, mediated through different immune mechanisms, can influence parasite fitness and how experimental manipulations of the immune system can be carried out to examine this. A better understanding of how parasite fitness scales with, or responds to, immunopathology is crucial to understanding the nature of selection acting on parasite virulence traits and will allow more informed predictions to be made regarding the trajectory of parasite virulence evolution.
Abstract.
Author URL.
Bacelar FS, White A, Boots M (2011). Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks.
Journal of Theoretical Biology,
269(1), 131-137.
Abstract:
Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks
tlsb-1%Males are often the 'sicker' sex with male biased parasitism found in a taxonomically diverse range of species. There is considerable interest in the processes that could underlie the evolution of sex-biased parasitism. Mating system differences along with differences in lifespan may play a key role. We examine whether these factors are likely to lead to male-biased parasitism through natural selection taking into account the critical role that ecological feedbacks play in the evolution of defence. We use a host-parasite model with two-sexes and the techniques of adaptive dynamics to investigate how mating system and sexual differences in competitive ability and longevity can select for a bias in the rates of parasitism. Male-biased parasitism is selected for when males have a shorter average lifespan or when males are subject to greater competition for resources. Male-biased parasitism evolves as a consequence of sexual differences in life-history that produce a greater proportion of susceptible females than males and therefore reduce the cost of avoiding parasitism in males. Different mating systems such as monogamy, polygyny or polyandry did not produce a bias in parasitism through these ecological feedbacks but may accentuate an existing bias. © 2010 Elsevier Ltd.
Abstract.
Best A, Webb S, Antonovics J, Boots M (2011). Local transmission processes and disease-driven host extinctions. Theoretical Ecology, 1-7.
Saejeng A, Siva-Jothy MT, Boots M (2011). Low cost antiviral activity of Plodia interpunctella haemolymph in vivo demonstrated by dose dependent infection.
Journal of Insect Physiology,
57(2), 246-250.
Abstract:
Low cost antiviral activity of Plodia interpunctella haemolymph in vivo demonstrated by dose dependent infection
Given the ubiquity of infectious disease it is important to understand the way in which hosts defend themselves and any costs that they may pay for this defence. Despite this, we know relatively little about insect immune responses to viruses when compared to their well-characterized responses to other pathogens. In particular it is unclear whether there is significant haemocoelic response to viral infection. Here we directly examine this question by examining whether there is a dose-dependency in infection risk when a DNA virus is injected directly into the haemocoel. Infection from direct injection into the haemocoel showed a clear dose dependency that is indicative of an active intrahaemocoelic immune response to DNA viruses in insects. In contrast to the natural oral infection route, we found no measurable sublethal effects in the survivours from direct injection. This suggests that the immune responses in the haemocoel are less costly than those that occur earlier. © 2010.
Abstract.
Leggett HC, Jones EO, Burke T, Hails RS, Sait SM, Boots M (2011). Population genetic structure of the winter moth, Operophtera brumata Linnaeus, in the Orkney Isles suggests long-distance dispersal.
Ecological Entomology,
36(3), 318-325.
Abstract:
Population genetic structure of the winter moth, Operophtera brumata Linnaeus, in the Orkney Isles suggests long-distance dispersal
The application of population genetic analysis and molecular ecological approaches allows us to examine the invasion of species in the wild. In particular, we can gain an insight into the role of dispersal, a key determinant of the invasion and population dynamics of important pest species. Since the 1980s, severe outbreaks of the winter moth, Operophtera brumata (Linnaeus), have caused extensive damage to heather moorlands in the Orkney Isles. The population genetic structure of O. brumata in Orkney was examined in order to establish whether the widely dispersed outbreaking populations are connected. Amplified fragment length polymorphism (AFLP) analysis showed a high level of genetic diversity within subpopulations. This is consistent with an initial mass colonisation event and/or continuing dispersal between populations of O. brumata in Orkney. Genetic differentiation among populations is low, and although some weak isolation by distance is detectable, no effect of isolation as a result of a sea barrier was found. High gene flow between populations is consistent with the low genetic differentiation observed, although there is evidence to suggest that the populations are not panmictic. Given the limited dispersal of adults, the present results suggest that larvae may disperse over considerable distances by ballooning on strong winds across the Orkney Isles. © 2011 the Authors. Ecological Entomology © 2011 the Royal Entomological Society.
Abstract.
Jones EO, White A, Boots M (2011). The evolution of host protection by vertically transmitted parasites.
Proc Biol Sci,
278(1707), 863-870.
Abstract:
The evolution of host protection by vertically transmitted parasites.
Hosts are often infected by a variety of different parasites, leading to competition for hosts and coevolution between parasite species. There is increasing evidence that some vertically transmitted parasitic symbionts may protect their hosts from further infection and that this protection may be an important reason for their persistence in nature. Here, we examine theoretically when protection is likely to evolve and its selective effects on other parasites. Our key result is that protection is most likely to evolve in response to horizontally transmitted parasites that cause a significant reduction in host fecundity. The preponderance of sterilizing horizontally transmitted parasites found in arthropods may therefore explain the evolution of protection seen by their symbionts. We also find that protection is more likely to evolve in response to highly transmissible parasites that cause intermediate, rather than high, virulence (increased death rate when infected). Furthermore, intermediate levels of protection select for faster, more virulent horizontally transmitted parasites, suggesting that protective symbionts may lead to the evolution of more virulent parasites in nature. When we allow for coevolution between the symbiont and the parasite, more protection is likely to evolve in the vertically transmitted symbionts of longer lived hosts. Therefore, if protection is found to be common in nature, it has the potential to be a major selective force on host-parasite interactions.
Abstract.
Author URL.
Boots M (2011). The evolution of resistance to a parasite is determined by resources.
Am Nat,
178(2), 214-220.
Abstract:
The evolution of resistance to a parasite is determined by resources.
Given the ubiquity of parasites, it is critical to understand the evolution of defense against them. Using a selection experiment performed across a broad range of host resources, I examine how resistance and associated costs depend on resource availability. Higher resistance to a natural viral pathogen evolves in a host when there are more resources, and this directly suggests a resource-dependent cost of the evolution of resistance. Resistance is traded off with host growth rate, and the costs are stronger under poor resource environments, although adaptation to poor environments reduces these costs. The level of resistance and the costs that are paid for this resistance depend on both the selection environment and the environment in which hosts are assayed, implying that different resistance mechanisms may evolve in different environments. More broadly, the results emphasize that environmental heterogeneity in time and space may underpin variation in immune diversity.
Abstract.
Author URL.
Laughton AM, Boots M, Siva-Jothy MT (2011). The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge.
J Insect Physiol,
57(7), 1023-1032.
Abstract:
The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge.
The honey bee, Apis mellifera, is an ideal system for investigating ontogenetic changes in the immune system, because it combines holometabolous development within a eusocial caste system. As adults, male and female bees are subject to differing selective pressures: worker bees (females) exhibit temporal polyethism, while the male drones invest in mating. They are further influenced by changes in the threat of pathogen infection at different life stages. We investigated the immune response of workers and drones at all developmental phases, from larvae through to late stage adults, assaying both a constitutive (phenoloxidase, PO activity) and induced (antimicrobial peptide, AMP) immune response. We found that larval bees have low levels of PO activity. Adult workers produced stronger immune responses than drones, and a greater plasticity in immune investment. Immune challenge resulted in lower levels of PO activity in adult workers, which may be due to the rapid utilisation and a subsequent failure to replenish the constitutive phenoloxidase. Both adult workers and drones responded to an immune challenge by producing higher titres of AMPs, suggesting that the cost of this response prohibits its constant maintenance. Both castes showed signs of senescence in immune investment in the AMP response. Different sexes and life stages therefore alter their immune system management based on the combined factors of disease risk and life history.
Abstract.
Author URL.
Reynolds JJH, White A, Sherratt JA, Boots M (2011). The population dynamical consequences of density-dependent prophylaxis.
Journal of Theoretical Biology,
288(1), 1-8.
Abstract:
The population dynamical consequences of density-dependent prophylaxis
When infectious disease transmission is density-dependent, the risk of infection will tend to increase with host population density. Since host defence mechanisms can be costly, individual hosts may benefit from increasing their investment in immunity in response to increasing population density. Such "density-dependent prophylaxis" (DDP) has now indeed been demonstrated experimentally in several species. However, it remains unclear how DDP will affect the population dynamics of the host-pathogen interaction, with previous theoretical work making conflicting predictions. We develop a general host-pathogen model and assess the role of DDP on the population dynamics. The ability of DDP to drive population cycles is critically dependent on the time delay between the change in density and the subsequent phenotypic change in the level of resistance. When the delay is absent or short, DDP destabilises the system. As the delay increases, its destabilising effect first diminishes and then DDP becomes increasingly stabilising. Our work highlights the significance of the time delay and suggests that it must be estimated experimentally or varied in theoretical investigations in order to understand the implications of DDP for the population dynamics of particular systems. © 2011 Elsevier Ltd.
Abstract.
Tidbury HJ, Pedersen AB, Boots M (2011). Within and transgenerational immune priming in an insect to a DNA virus.
Proc Biol Sci,
278(1707), 871-876.
Abstract:
Within and transgenerational immune priming in an insect to a DNA virus.
Invertebrates mount a sophisticated immune response with the potential to exhibit a form of immune memory through 'priming'. Increased immune protection following early exposure to bacteria has been found both later in life (within generation priming) and in the next generation (transgeneration priming) in a number of invertebrates. However, it is unclear how general immune priming is and whether immune priming occurs in response to different parasites, including viruses. Here, using Plodia interpuctella (Lepidoptera) and its natural DNA virus, Plodia interpunctella granulosis virus, we find evidence for both within generation and transgeneration immune priming. Individuals previously exposed to low doses of virus, as well as the offspring of exposed individuals, are subsequently less susceptible to viral challenge. Relatively little is known about the mechanisms that underpin viral immunity but it is probable that the viral immune response is somewhat different to that of bacteria. We show that immune priming may, however, be a characteristic of both responses, mediated through different mechanisms, suggesting that immune memory may be a general phenomenon of insect immunity. This is important because immune priming may influence both host-parasite population and evolutionary dynamics.
Abstract.
Author URL.
2010
Lion S, Boots M (2010). Are parasites ''prudent'' in space?.
Ecology Letters,
13(10), 1245-1255.
Abstract:
Are parasites ''prudent'' in space?
Ecology Letters (2010)There has been a renewed controversy on the processes that determine evolution in spatially structured populations. Recent theoretical and empirical studies have suggested that parasites should be expected to be more ''prudent'' (less harmful and slower transmitting) when infection occurs locally. Using a novel approach based on spatial moment equations, we show that the evolution of parasites in spatially structured host populations is determined by the interplay of genetic and demographic spatial structuring, which in turn depends on the details of the ecological dynamics. This allows a detailed understanding of the roles of epidemiology, demography and network topology. Demographic turnover is needed for local interactions to select for prudence in the susceptible-infected models that have been the focus of previous studies. In diseases with little demographic turnover (as typical of many human diseases), we show that only parasites causing diseases with long-lived immunity are likely to be prudent in space. We further demonstrate why, at intermediate parasite dispersal, virulence can evolve to higher levels than predicted by non-spatial theory. © 2010 Blackwell Publishing Ltd/CNRS.
Abstract.
Abu Hassan A, Dieng H, Satho T, Boots M, Al Sariy JSL (2010). Breeding patterns of the JE vector Culex gelidus and its insect predators in rice cultivation areas of northern peninsular Malaysia.
Tropical Biomedicine,
27(3), 404-416.
Abstract:
Breeding patterns of the JE vector Culex gelidus and its insect predators in rice cultivation areas of northern peninsular Malaysia
Japanese encephalitis (JE) virus activity is an important cause of viral encephalitis in Southeast Asia. In Malaysia, JEV activity has been first detected in Culex gelidus in 1976. Since then, no study has fully addressed the seasonal dynamics of this mosquito. As irrigated rice production expands, the incidence of JEV vectors, particularly Cx. gelidus is expected to increase. We surveyed Penang Island to determine the breeding patterns of Cx. gelidus and their potential insect predators, in relation to habitat/niche and rice growing period. Six rice fields proper (RFP) and related drainage canals (DC) were visited through three cultivation cycles (CCs) over 17 months. Weekly visits were performed to each of the 36 sites and mosquito larvae and aquatic insects were sampled from RFP and DCs using dippers. Culex gelidus was abundant in RFP and almost absent in DCs. Its densities usually were high during the first and 3rd CC and when the RFs were in Fp, Pp and Gp. In DCs, the mosquito was abundant during Mp, e.g. 2nd CC. Predators, especially those belonging to the families Corixidae, Coenagrionidae and Dytiscidae, were more present in RFP. Predator numbers usually were high during the first CC; in some cases predator abundance peaked during other CCs, e.g. corixids and dysticids. In RFP, neither corixids nor coenagrionids showed any positive correlation with densities of Cx. gelidus. However, dytiscids' population peaked when the mosquito densities were on the rise. These observations suggest that Cx. gelidus is active during the period of rice cultivation. Operational vector control through bio-control or with insecticides near the end of the rice cultivation season in RFP may prove beneficial in reducing the density of Cx. gelidus, but also the amount of bio-agent or insecticide applied on riceland.
Abstract.
Rudolf VHW, Kamo M, Boots M (2010). Cannibals in space: the coevolution of cannibalism and dispersal in spatially structured populations.
American Naturalist,
175(5), 513-524.
Abstract:
Cannibals in space: the coevolution of cannibalism and dispersal in spatially structured populations
The propensity for cannibalism varies considerably both within and between species. Currently we have little understanding of both the causes of this variation and its evolutionary consequences for other life-history traits. We examine how different levels of spatial structure affect the evolution of cannibalism and how cannibalism in turn drives the evolution of dispersal. Using pair approximations and simulations, we show that cannibalism can easily evolve in spatially structured populations as long as some dispersal exists. Furthermore, for a wide range of intermediate levels of spatial structure, we find the possibility of evolutionary branching leading to polymorphism in cannibalism. We also show that cannibalism itself can have important evolutionary consequences and select for increased dispersal rates, thus helping to determine the spatial structure of populations. The coevolution of cannibalism and dispersal results in the evolution of various alternative life-history strategies with different dispersal and cannibalism regimes. Which strategy evolves depends on the environmental conditions that determine initial cannibalism rates. Our results therefore suggest that differences in spatial structure could explain variation in the propensity for cannibalism and cannibalistic polyphenism. Furthermore, results emphasize that cannibalism can drive the evolution of other life-history traits and determine the spatial structure of natural populations. © 2010 by the University of Chicago.
Abstract.
Saejeng A, Tidbury H, Siva-Jothy MT, Boots M (2010). Examining the relationship between hemolymph phenoloxidase and resistance to a DNA virus, Plodia interpunctella granulosis virus (PiGV).
Journal of Insect Physiology,
56(9), 1232-1236.
Abstract:
Examining the relationship between hemolymph phenoloxidase and resistance to a DNA virus, Plodia interpunctella granulosis virus (PiGV)
We have a detailed understanding of invertebrate immune responses to bacteria and fungal pathogens, but we know less about how insects respond to virus challenge. Phenoloxidase (PO) functions as an important immune response against many parasites and pathogens and is routinely used as a measure of immune competance. We examine the role of haemolymph PO activity in Plodia interpuncetella's response to its natural granulosis virus (PiGV). Larvae were challenged with virus by both oral inoculation of occluded virus (the natural infection route) and direct intrahaemocoelic injection of budded virus. Haemolymph was collected at time points post-viral challenge using a novel method that allows the volume of haemolymph to be quanitified. The haemolmyph was collected without killing the larvae so that haemolymph samples from individuals that developed viral disease could be distinguished from samples collected from those that fought off infection. The level of haemolymph PO activity in resistant larvae did not differ from control larvae. Therefore we have no evidence that PO is involved in resistance to virus in the haemocoel whether larvae are challenged naturally by oral innoculation or directly by intraheamocoelic injection. Phenoloxidase may therefore not be a relevant metric of immunocompetence for viral infection. © 2010 Elsevier Ltd.
Abstract.
Adams B, Boots M (2010). How important is vertical transmission in mosquitoes for the persistence of dengue? Insights from a mathematical model.
EPIDEMICS,
2(1), 1-10.
Author URL.
Dieng H, Saifur RGM, Hassan AA, Che Salmah MR, Boots M, Satho T, Jaal Z, Abubakar S (2010). Indoor-breeding of Aedes albopictus in northern peninsular Malaysia and its potential epidemiological implications.
PLoS ONE,
5(7).
Abstract:
Indoor-breeding of Aedes albopictus in northern peninsular Malaysia and its potential epidemiological implications
Background: the mosquito Ae. albopictus is usually adapted to the peri-domestic environment and typically breeds outdoors. However, we observed its larvae in most containers within homes in northern peninsular Malaysia. To anticipate the epidemiological implications of this indoor-breeding, we assessed some fitness traits affecting vectorial capacity during colonization process. Specifically, we examined whether Ae. albopictus exhibits increased survival, gonotrophic activity and fecundity due to the potential increase in blood feeding opportunities. Methodology/Principal Findings: in a series of experiments involving outdoors and indoors breeding populations, we found that Ae. albopictus lives longer in the indoor environment. We also observed increased nighttime biting activity and lifetime fecundity in indoor/domestic adapted females, although they were similar to recently colonized females in body size. Conclusion/Significance: Taken together these data suggest that accommodation of Ae. albopictus to indoor/domestic environment may increase its lifespan, blood feeding success, nuisance and thus vectorial capacity (both in terms of increased vector-host contacts and vector population density). These changes in the breeding behavior of Ae. albopictus, a potential vector of several human pathogens including dengue viruses, require special attention. © 2010 Dieng et al.
Abstract.
Bacelar FS, White A, Boots M (2010). Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks.
Best A, White A, Boots M (2010). Resistance is futile but tolerance can explain why parasites do not always castrate their hosts.
Evolution,
64(2), 348-357.
Abstract:
Resistance is futile but tolerance can explain why parasites do not always castrate their hosts.
The disease caused by parasites and pathogens often causes sublethal effects that reduce host fecundity. Theory suggests that if parasites can "target" the detrimental effects of their growth on either host mortality or fecundity, they should always fully sterilize. This is because a reduction in host fecundity does not reduce the infectious period and is therefore neutral to a horizontally transmitted infectious organism. However, in nature fully castrating parasites are relatively rare, no doubt in part because of defense mechanisms in the host. Here, we examine in detail the evolution of host defense to the sterilizing effects of parasites and show that intermediate levels of sterility tolerance are found to evolve for a wide range of cost structures. Our key result arises when the host and parasite coevolve. Investment in tolerance by the host may prevent castration, but if host defense is through resistance (by controlling the parasite's growth rate) coevolution by the parasite results in the complete loss of infected host fecundity. Resistance is therefore a waste of resources, but tolerance can explain why parasites do not castrate their hosts. Our results further emphasize the importance of tolerance as opposed to resistance to parasites.
Abstract.
Author URL.
Saifur RGM, Dieng H, Hassan AA, Satho T, Miake F, Boots M, Salmah MRC, Abubakar S (2010). The effects of moisture on ovipositional responses and larval eclosion of Aedes albopictus.
Journal of the American Mosquito Control Association,
26(4), 373-380.
Abstract:
The effects of moisture on ovipositional responses and larval eclosion of Aedes albopictus
Moisture plays a major role in the dynamics of mosquito populations, especially those breeding in container habitats. Despite this importance, the role of moisture conditions as they affect oviposition and egg development in Aedes vectors remains largely unexplored. We investigated the effect of exposing gravid female Aedes albopictus mosquitoes and their eggs to different moisture levels (MLs) for various periods on oviposition and hatching. Overall, high-moisture substrates (HMSs; 66% and 72%) provided better environments for egg laying. The timing of initial egg laying was far longer at the lowest substrate moisture level (LSML, 25% and 41.2%) than at HMSs. The numbers of eggs laid were much lower in the drier environments. At LSMLs, gravid females retained increasing numbers of mature eggs until death, and egg retention decreased gradually with increasing ML. The HMSs also provided better environments for larval eclosion. The numbers of eggs hatched were lower at the LSML than the HSML environment. No egg hatching occurred after 1 h exposure to moisture. However, egg hatching occurred by installment, with spontaneous hatching (SH) increasing gradually with increasing ML. High-moisture conditions combined with long exposure (30 h and 48 h) favored SH. These results suggest that Ae. albopictus females can respond to better moisture conditions for increased success of embryonation and larval eclosion. This information may be useful in the colonization of floodwater Aedes species. © 2010 by the American Mosquito Control Association, Inc.
Abstract.
Best A, White A, Kisdi E, Antonovics J, Brockhurst MA, Boots M (2010). The evolution of host-parasite range.
Am Nat,
176(1), 63-71.
Abstract:
The evolution of host-parasite range.
Understanding the coevolution of hosts and parasites is one of the key challenges for evolutionary biology. In particular, it is important to understand the processes that generate and maintain variation. Here, we examine a coevolutionary model of hosts and parasites where infection does not depend on absolute rates of transmission and defense but is approximately all-or-nothing, depending on the relative levels of defense and infectivity of the host and the parasite. We show that considerable diversity can be generated and maintained because of epidemiological feedbacks, with strains differing in the range of host and parasite types they can respectively infect or resist. Parasites with broad and narrow ranges therefore coexist, as do broadly and narrowly resistant hosts, but this diversity occurs without the assumption of highly specific gene interactions. In contrast to gene-for-gene models, cycling in strain types is found only under a restrictive set of circumstances. The generation of diversity in both hosts and parasites is dependent on the shape of the trade-off relationships but is more likely in long-lived hosts and chronic disease with long infectious periods. Overall, our model shows that significant diversity in infectivity and resistance range can evolve and be maintained from initially monomorphic populations.
Abstract.
Author URL.
Jones EO, White A, Boots M (2010). The evolutionary implications of conflict between parasites with different transmission modes.
Evolution,
64(8), 2408-2416.
Abstract:
The evolutionary implications of conflict between parasites with different transmission modes.
Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life-history trade-offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short-lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study.
Abstract.
Author URL.
Childs DZ, Boots M (2010). The interaction of seasonal forcing and immunity and the resonance dynamics of malaria.
J R Soc Interface,
7(43), 309-319.
Abstract:
The interaction of seasonal forcing and immunity and the resonance dynamics of malaria.
Theory has emphasized the importance of both intrinsic factors such as host immunity and extrinsic drivers such as climate in determining disease dynamics. In particular, seasonality may lead to multi-annual cycles in prevalence, but the likelihood of this depends on the role of acquired immunity. Some diseases including malaria have immunity that falls between the classic susceptible-infectious-removed and susceptible-infectious-susceptible models. Here, we investigate the general conditions promoting the subharmonic resonance behaviour that may lead to multi-annual cycles in a general malaria dynamical model. Utilizing two complementary approaches to bifurcation analyses, we show that resonance is promoted by processes shortening the length of the infectious period and that subharmonic cycles are favoured in situations with strong seasonality in transmission but at intermediate levels of endemicity. We discuss the implications of our results for understanding prevalence patterns in long-term malaria datasets from Kenya that show multi-annual cycles and one from Thailand that does not and discuss the possible implications of treatment.
Abstract.
Author URL.
2009
Bell SS, White A, Sherratt JA, Boots M (2009). Invading with biological weapons: the role of shared disease in ecological invasion.
Theoretical Ecology,
2(1), 53-66.
Abstract:
Invading with biological weapons: the role of shared disease in ecological invasion
Theory has been developed that examines the role of infectious disease in ecological invasions for particular natural systems. However, a general understanding of the role that shared disease may play in invasions is lacking. Here, we develop a strategic theoretical framework to determine the role of disease, in addition to competition, in ecological invasions and the expansion of species' spatial range. We investigate the effect of different disease parameters on the replacement time of a native species by an alien invader. The outcome is critically dependent on the relative effects that the disease has on the two species and less dependent on the basic epidemiological characteristics of the interaction. This framework is also used to investigate the effect of disease on the spatial spread of the invader. Our results show an interesting phenomenon where a wave of disease spreads through the landscape ahead of the wave of replacement. © Springer Science+Business Media B.V. 2008.
Abstract.
Boots M, Childs D, Reuman DC, Mealor M (2009). Local interactions lead to pathogen-driven change to host population dynamics.
Curr Biol,
19(19), 1660-1664.
Abstract:
Local interactions lead to pathogen-driven change to host population dynamics.
Individuals tend to interact more strongly with nearby individuals or within particular social groups. Recent theoretical advances have demonstrated that these within-population relationships can have fundamental implications for ecological and evolutionary dynamics. In particular, contact networks are crucial to the spread and evolution of disease. However, the theory remains largely untested experimentally. Here, we manipulate habitat viscosity and thereby the frequency of local interactions in an insect-pathogen model system in which the virus had previously been shown to have little effect on host population dynamics. At high viscosity, the pathogen caused the collapse of dominant and otherwise stable host generation cycles. Modeling shows that this collapse can be explained by an increase in the frequency of intracohort interactions relative to intercohort interactions, leading to more disease transmission. Our work emphasizes that spatial structure can subtly mediate intraspecific competition and the effects of natural enemies. A decrease in dispersal in a population may actually (sometimes rather counterintuitively) intensify the effects of parasites. Broadly, because anthropological and environmental change often cause changes in population mixing, our work highlights the potential for dramatic changes in the effects of parasites on host populations.
Abstract.
Author URL.
Sorrell I, White A, Pedersen AB, Hails RS, Boots M (2009). The evolution of covert, silent infection as a parasite strategy.
Proc Biol Sci,
276(1665), 2217-2226.
Abstract:
The evolution of covert, silent infection as a parasite strategy.
Many parasites and pathogens cause silent/covert infections in addition to the more obvious infectious disease-causing pathology. Here, we consider how assumptions concerning superinfection, protection and seasonal host birth and transmission rates affect the evolution of such covert infections as a parasite strategy. Regardless of whether there is vertical infection or effects on sterility, overt infection is always disadvantageous in relatively constant host populations unless it provides protection from superinfection. If covert infections are protective, all individuals will enter the covert stage if there is enough vertical transmission, and revert to overt infections after a 'latent' period (susceptible, exposed, infected epidemiology). Seasonal variation in transmission rates selects for non-protective covert infections in relatively long-lived hosts with low birth rates typical of many mammals. Variable host population density caused by seasonal birth rates may also select for covert transmission, but in this case it is most likely in short-lived fecund hosts. The covert infections of some insects may therefore be explained by their outbreak population dynamics. However, our models consistently predict proportions of covert infection, which are lower than some of those observed in nature. Higher proportions of covert infection may occur if there is a direct link between covert infection and overt transmission success, the covert infection is protective or the covert state is the result of suppression by the host. Relatively low proportions of covert transmission may, however, be explained as a parasite strategy when transmission opportunities vary.
Abstract.
Author URL.
Best A, White A, Boots M (2009). The implications of coevolutionary dynamics to host-parasite interactions.
Am Nat,
173(6), 779-791.
Abstract:
The implications of coevolutionary dynamics to host-parasite interactions.
Due to the importance of infectious disease, there is a large body of theory on the evolution of either hosts or, more commonly, parasites. Here we present a fully coevolutionary model of a host-parasite system that includes ecological dynamics that feed back into the coevolutionary outcome, and we show that highly virulent parasites may evolve due to the coevolutionary process. Parasite evolution is very sensitive to evolution in the host, and virulence fluctuates substantially when mutation rates vary between host and parasite. Evolutionary branching in the host leads to parasites increasing their virulence, and small changes in host resistance drive large changes in parasite virulence. Evolutionary branching in one species does not cause branching in the other. Our work emphasizes the importance of considering coevolutionary dynamics and shows that certain highly virulent parasites may result from responses to host evolution.
Abstract.
Author URL.
Boots M, Best A, Miller MR, White A (2009). The role of ecological feedbacks in the evolution of host defence: what does theory tell us?.
Philos Trans R Soc Lond B Biol Sci,
364(1513), 27-36.
Abstract:
The role of ecological feedbacks in the evolution of host defence: what does theory tell us?
Hosts have evolved a diverse range of defence mechanisms in response to challenge by infectious organisms (parasites and pathogens). Whether defence is through avoidance of infection, control of the growth of the parasite once infected, clearance of the infection, tolerance to the disease caused by infection or innate and/or acquired immunity, it will have important implications for the population ecology (epidemiology) of the host-parasite interaction. As a consequence, it is important to understand the evolutionary dynamics of defence in the light of the ecological feedbacks that are intrinsic to the interaction. Here, we review the theoretical models that examine how these feedbacks influence the nature and extent of the defence that will evolve. We begin by briefly comparing different evolutionary modelling approaches and discuss in detail the modern game theoretical approach (adaptive dynamics) that allows ecological feedbacks to be taken into account. Next, we discuss a number of models of host defence in detail and, in particular, make a distinction between 'resistance' and 'tolerance'. Finally, we discuss coevolutionary models and the potential use of models that include genetic and game theoretical approaches. Our aim is to review theoretical approaches that investigate the evolution of defence and to explain how the type of defence and the costs associated with its acquisition are important in determining the level of defence that evolves.
Abstract.
Author URL.
2008
Boots M (2008). Fight or learn to live with the consequences?.
Trends Ecol Evol,
23(5), 248-250.
Abstract:
Fight or learn to live with the consequences?
Individuals can fight their infectious diseases by reducing the growth of a pathogen (resistance), but they can also ameliorate the disease it causes (tolerance). A recent paper shows that there is variation between mouse strains in tolerance to a rodent malaria and that this was negatively correlated with resistance. This is important, because tolerance has major implications for the epidemiology and coevolution of host-parasite interactions, but has been neglected in the animal literature.
Abstract.
Author URL.
Best A, White A, Boots M (2008). Maintenance of host variation in tolerance to pathogens and parasites.
Proc Natl Acad Sci U S A,
105(52), 20786-20791.
Abstract:
Maintenance of host variation in tolerance to pathogens and parasites.
Tolerance and resistance provide hosts with two distinct defense strategies against parasitism. In resistance the hosts "fight" the parasite directly, whereas in tolerance the hosts fight the disease by ameliorating the damage that infection causes. There is increasing recognition that the two mechanisms may exhibit very different evolutionary behaviors. Although empirical work has often noted considerable variance in tolerance within hosts, theory has predicted the fixation of tolerance due to positive frequency dependence through a feedback with disease prevalence. Here we reconcile these findings through a series of dynamic game theoretical models. We emphasize that there is a crucial distinction between tolerance to the effects of disease-induced mortality and tolerance to the effect of the disease-induced reductions in fecundity. Only mortality tolerance has a positive effect on parasite fitness, whereas sterility tolerance is neutral and may therefore result in polymorphisms. The nature of the costs to defense and their relationship to trade-offs between resistance and tolerance are crucial in determining the likelihood of variation, whereas the co-evolution of the parasite will not affect diversity. Our findings stress that it is important to measure the effects of different mechanisms on characteristics that affect the epidemiology of the parasite to completely understand the evolutionary dynamics of defense.
Abstract.
Author URL.
Hoyle A, Bowers RG, White A, Boots M (2008). The influence of trade-off shape on evolutionary behaviour in classical ecological scenarios.
J Theor Biol,
250(3), 498-511.
Abstract:
The influence of trade-off shape on evolutionary behaviour in classical ecological scenarios.
Trade-off shapes are crucial to evolutionary outcomes. However, due to different ecological feedbacks their implications may depend not only on the trade-off being considered but also the ecological scenario. Here, we apply a novel geometric technique, trade-off and invasion plots (TIPs), to examine in detail how the shape of trade-off relationships affect evolutionary outcomes under a range of classic ecological scenarios including Lotka-Volterra type and host-parasite interactions. We choose models of increasing complexity in order to gain an insight into the features of ecological systems that determine the evolutionary outcomes. In particular we focus on when evolutionary attractors, repellors and branching points occur and how this depends on whether the costs are accelerating (benefits become 'increasingly' costly), decelerating (benefits become 'decreasingly' costly) or constant. In all cases strongly accelerating costs lead to attractors while strongly decelerating ones lead to repellors, but with weaker relationships, this no longer holds. For some systems weakly accelerating costs may lead to repellors and decelerating costs may lead to attractors. In many scenarios it is weakly decelerating costs that lead to branching points, but weakly accelerating and linear costs may also lead to disruptive selection in particular ecological scenarios. Using our models we suggest a classification of ecological interactions, based on three distinct criteria, that can produce one of four fundamental TIPs which allow for different evolutionary behaviour. This provides a baseline theory which may inform the prediction of evolutionary outcomes in similar yet unexplored ecological scenarios. In addition we discuss the implications of our results to a number of specific life-history trade-offs in the classic ecological scenarios represented by our models.
Abstract.
Author URL.
Hamilton R, Siva-Jothy M, Boots M (2008). Two arms are better than one: parasite variation leads to combined inducible and constitutive innate immune responses.
Proc Biol Sci,
275(1637), 937-945.
Abstract:
Two arms are better than one: parasite variation leads to combined inducible and constitutive innate immune responses.
Parasites represent a major threat to all organisms which has led to the evolution of an array of complex and effective defence mechanisms. Common to both vertebrates and invertebrates are innate immune mechanisms that can be either constitutively expressed or induced on exposure to infection. In nature, we find that a combination of both induced and constitutive responses are employed by vertebrates, invertebrates and, to an extent, plants when they are exposed to a parasite. Here we use a simple within-host model motivated by the insect immune system, consisting of both constitutive and induced responses, to address the question of why both types of response are maintained so ubiquitously. Generally, induced responses are thought to be advantageous because they are only used when required but are too costly to maintain constantly, while constitutive responses are advantageous because they are always ready to act. However, using a simple cost function but with no a priori assumptions about relative costs, we show that variability in parasite growth rates selects for a strategy that combines both constitutive and induced defences. Differential costs are therefore not necessary to explain the adoption of both forms of defence. Clearly, hosts are likely to be challenged by variable parasites in nature and this is sufficient to explain why it is optimal to deploy both arms of the innate immune system.
Abstract.
Author URL.
2007
Dieng H, Boots M, Higashihara J, Okada T, Kato K, Satho T, Miake F, Eshita Y (2007). Effects of blood and virus-infected blood on protein expression in the midgut of the dengue vector Aedes albopictus.
Medical and Veterinary Entomology,
21(3), 278-283.
Abstract:
Effects of blood and virus-infected blood on protein expression in the midgut of the dengue vector Aedes albopictus
Although the mosquito midgut is the primary site of bloodmeal storage and the first line of defence against pathogenic infection, little is known about its proteic composition at a time when an increasing number of proteins are reported to impair viral infection. Aedes albopictus Skuse (Diptera: Culicidae) is an important vector of the dengue virus. We compared 2-dimensional protein profiles of the adult midgut in this species, taking into account bloodmeal status. The comparison of profiles from sugar-fed and blood-fed females showed that a considerable number of proteins were present in both midguts. In addition, one set of proteins was present only after sugar intake and another set only after blood intake. The comparison of profiles of blood-fed midguts and dengue virus-2 infected blood-fed midguts revealed that at least six proteins were present only in the infected midguts. These results are discussed in the context of the identification of midgut proteins involved in the dengue virus infection process. © 2007 the Royal Entomological Society.
Abstract.
Miller MR, White A, Boots M (2007). Host life span and the evolution of resistance characteristics.
Evolution,
61(1), 2-14.
Abstract:
Host life span and the evolution of resistance characteristics.
There is a wide variety of resistance mechanisms that hosts may evolve in response to their parasites. These can be functionally classified as avoidance (lower probability of becoming infected), recovery (faster rate of clearance), tolerance (reduced death rate when infected), or acquired immunity. It is commonly thought that longer lived organisms should invest more in costly resistance. We show that due to epidemiological feedbacks the situation is often more complex. Using evolutionary theory we examine how the optimal investment in costly resistance varies with life span in a broad range of scenarios. In the absence of acquired immunity, longer lived populations do generally invest more in resistance. If hosts have acquired immunity, the optimal resistance may either increase or decrease with increasing life span. In addition, there may be evolutionary bistability with high and low investments in avoidance or tolerance. The optimal investment in the duration of acquired immunity always increases with life span, and due to bistability, shorter lived hosts may commonly not evolve any immunity. In contrast, the optimal investment in the probability of acquiring immunity initially increases and then decreases with life span. Our results have important implications for the evolution of invertebrate and vertebrate immunity, and for the evolution of acquired immunity itself.
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Author URL.
Webb SD, Keeling MJ, Boots M (2007). Host-parasite interactions between the local and the mean-field: how and when does spatial population structure matter?.
J Theor Biol,
249(1), 140-152.
Abstract:
Host-parasite interactions between the local and the mean-field: how and when does spatial population structure matter?
The assumption that populations are completely mixed is reasonable for many populations, but there is likely to be some degree of local interaction whether spatially or socially in many systems. An important question is therefore how strong these local interactions need to be before there are significant effects on the dynamics of the system. Here, our approach is to use a multi-scale pair-approximation model to move between completely local and completely mixed host-parasite interactions. We show that systems dominated by near neighbour effects have less persistence of disease, and a greater possibility of parasite driven extinction and limit cycles. Furthermore this reduction in persistence occurs over a wide range of infection scales and is still significant in predominantly mixed host populations. Deterministic extinctions are only likely in highly spatial SI systems while oscillations also persist over a wide range of infection ranges, but only in hosts that reproduce mostly locally. In general the mean-field may well be a good approximation for many systems, even when there are a significant proportion of near neighbour events, but this depends crucially on the ecological context.
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Author URL.
Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007). Host-parasite population dynamics under combined frequency- and density-dependent transmission.
Oikos,
116(12), 2017-2026.
Abstract:
Host-parasite population dynamics under combined frequency- and density-dependent transmission
Many host-parasite models assume that transmission increases linearly with host population density ('density-dependent transmission'), but various alternative transmission functions have been proposed in an effort to capture the complexity of real biological systems. The most common alternative (usually applied to sexually transmitted parasites) assumes instead that the rate at which hosts contact one another is independent of population density, leading to 'frequency-dependent' transmission. This straight-forward distinction generates fundamentally different dynamics (e.g. deterministic, parasite-driven extinction with frequency- but not density-dependence). Here, we consider the situation where transmission occurs through two different types of contact, one of which is density-dependent (e.g. social contacts), the other density-independent (e.g. sexual contacts). Drawing on a range of biological examples, we propose that this type of contact structure may be widespread in natural populations. When our model is characterized mainly by density-dependent transmission, we find that allowing even small amounts of transmission to occur through density-independent contacts leads to the possibility of deterministic, parasite-driven extinction (and lowers the threshold for parasite persistence). Contrastingly, allowing some density-dependent transmission to occur in a model characterized mainly by density-independent contacts (i.e. by frequency-dependent transmission) does not affect the extinction threshold, but does increase the likelihood of parasite persistence. The idea that directly transmitted parasites exploit different types of host contact is not new, but here we show that the impact on dynamics can be fundamental even in the simplest cases. For example, in systems where density-dependent transmission is normally assumed de facto, we show that parasite-driven extinction can occur if a small amount of transmission occurs through density-independent contacts. Many empirical studies are still guided by the traditional density/frequency dichotomy, but our combined transmission function may provide a better model for systems in which both types of transmission occur. © the Authors.
Abstract.
Jones EO, White A, Boots M (2007). Interference and the persistence of vertically transmitted parasites.
J Theor Biol,
246(1), 10-17.
Abstract:
Interference and the persistence of vertically transmitted parasites.
Given their ubiquity in nature, understanding the factors that allow the persistence of multiple enemies and in particular vertically transmitted parasites (VTPs) is of considerable importance. Here a model that allows a virulent VTP to be maintained in a system containing a host and a horizontally transmitted parasite (HTP) is analysed. The method of persistence relies on the VTP offering the host a level of protection from the HTP. The VTP is assumed to reduce the HTPs ability to transmit to the host through ecological interference. We show that VTPs are more likely to persist with HTPs that prevent host reproduction than with those that allow it. The VTP persists more easily in r-selected hosts and with highly transmittable HTPs. As the level of protection through interference increases the densities of the host also increase. We also show that VTPs when they do persist tend to stabilise the host population cycles produced by free-living HTPs. The study raised questions about persistence of diseases through interactions with others, and also the stabilising effects of VTPs on dynamical systems in a biological control context.
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Author URL.
Boots M, Mealor M (2007). Local interactions select for lower pathogen infectivity.
Science,
315(5816), 1284-1286.
Abstract:
Local interactions select for lower pathogen infectivity.
Theory suggests that the current rapid increase in connectivity and consequential changes in the structure of human, agricultural, and wildlife populations may select for parasite strains with higher infectivity. We carried out a test of this spatial theory by experimentally altering individual host movement rates in a model host/pathogen system by altering the viscosity of their environment. In our microevolutionary selection experiments, the infectivity of the virus was, as predicted by the theory, reduced in the most viscous populations. We therefore provide empirical support for the theory that population structure affects the evolution of infectious organisms.
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Author URL.
Webb SD, Keeling MJ, Boots M (2007). Spatially extended host-parasite interactions: the role of recovery and immunity.
Theor Popul Biol,
71(2), 251-266.
Abstract:
Spatially extended host-parasite interactions: the role of recovery and immunity.
Techniques for determining the long-term dynamics of host-parasite systems are well established for mixed populations. The field of spatial modelling in ecology is more recent but a number of key advances have been made. In this paper, we use state-of-the-art approximation techniques, supported by simulations, in order to investigate the role of recovery and immunity in spatially structured populations. Our approach is to use correlation models, namely pair-wise models, to capture the spatial relationships of contacts and interactions between individuals. We use the pair-wise framework to address a number of key ecological questions; including, the persistence of endemic limit cycles and regions of parasite-driven extinction--features which differentiate spatial from non-spatial models--and the effects on invasion fitness. We demonstrate a loss of limit cycle behaviour, in addition to an increase in the critical transmissibility and extinction thresholds, when recovery is included. This approach allows for a better analytical understanding of the dynamics of host-parasite interactions and demonstrates the importance of recovery and immunity in local interactions.
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Author URL.
Adams B, Boots M (2007). The influence of immune cross-reaction on phase structure in resonant solutions of a multi-strain seasonal SIR model.
J Theor Biol,
248(1), 202-211.
Abstract:
The influence of immune cross-reaction on phase structure in resonant solutions of a multi-strain seasonal SIR model.
Resonance in seasonally forced SIR epidemiological models may lead to stable solutions in which the epidemic period is an integer multiple of the forcing period. We examine the influence of immune cross-protection and cross-enhancement on the epidemic phase relationship of resonance solutions in an annually forced two-strain SIR model. Solutions with epidemics of the two strains in-phase commonly occur for wide ranges of cross-reaction intensity. Solutions with epidemics out-of-phase are less common and limited to narrow ranges of cross-reaction intensity. This is broadly as predicted by the two natural periods of the system. The natural period corresponding to out-of-phase solutions is sensitive to changes in the cross-reaction parameter but the natural period corresponding to in-phase solutions is constant. Bifurcation analysis indicates that the stability of in-phase orbits is controlled by pitchfork and period doubling bifurcations while out-of-phase orbits may also be influenced by Andronov-Hopf bifurcations. In order to develop an intuitive understanding of the epidemiological factors governing the occurrence of different solutions we consider how the susceptible, infected and removed components of the system must interact to form a stable solution. This shows that the impact of cross-reaction is moderated by in-phase structures but amplified by out-of-phase structures. Although the average infection rate over long time periods is not affected by phase structure, this analysis indicates that in-phase epidemic patterns are likely to be more consistent and thus allow more effective health care management.
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Author URL.
Miller MR, White A, Wilson K, Boots M (2007). The population dynamical implications of male-biased parasitism in different mating systems.
PLoS One,
2(7).
Abstract:
The population dynamical implications of male-biased parasitism in different mating systems.
Although there is growing evidence that males tend to suffer higher levels of parasitism than females, the implications of this for the population dynamics of the host population are not yet understood. Here we build on an established 'two-sex' model and investigate how increased susceptibility to infection in males affects the dynamics, under different mating systems. We investigate the effect of pathogenic disease at different case mortalities, under both monogamous and polygynous mating systems. If the case mortality is low, then male-biased parasitism appears similar to unbiased parasitism in terms of its effect on the population dynamics. At higher case mortalities, we identified significant differences between male-biased and unbiased parasitism. A host population may therefore be differentially affected by male-biased and unbiased parasitism. The dynamical outcome is likely to depend on a complex interaction between the host's mating system and demography, and the parasite virulence.
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Author URL.
Kamo M, Sasaki A, Boots M (2007). The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach.
Journal of Theoretical Biology,
244(4), 588-596.
Abstract:
The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach
Given the substantial changes in mixing in many populations, there is considerable interest in the role that spatial structure can play in the evolution of disease. Here we examine the role of different trade-off shapes in the evolution of parasites in a spatially structured host population where infection can occur locally or globally. We develop an approximate adaptive dynamic analytical approach, to examine how the evolutionarily stable (ES) virulence depends not only on the fraction of global infection/transmission but also on the shape of the trade-off between transmission and virulence. Our analysis can successfully predict the ES virulence found previously by simulation of the full system. The analysis confirms that when there is a linear trade-off between transmission and virulence spatial structure may lead to an ES virulence that increases as the proportion of global transmission increases. However, we also show that the ESS disappears above a threshold level of global infection, leading to maximization. In addition just below this threshold, there is the possibility of evolutionary bi-stabilities. When we assume the realistic trade-off between transmission and virulence that results in an ESS in the classical mixed model, we find that spatial structure can increase or decrease the ES virulence. A relatively high proportion of local infection reduces virulence but intermediate levels can select for higher virulence. Our work not only emphasizes the importance of spatial structure to the evolution of parasites, but also makes it clear that situations between the local and the global need to be considered. We also emphasize the key role that the shape of trade-offs plays in evolutionary outcomes. © 2006 Elsevier Ltd. All rights reserved.
Abstract.
Beckerman AP, Boots M, Gaston KJ (2007). Urban bird declines and the fear of cats.
Animal Conservation,
10(3), 320-325.
Abstract:
Urban bird declines and the fear of cats
The role of domestic cats Felis catus in the troubling, on-going decline of many urban bird populations in the UK is controversial. Debate, in the UK and elsewhere, has centred on the level of avian mortality directly imposed by cats, and on whether this is principally compensatory (the 'doomed surplus' hypothesis) or additive (the 'hapless survivor' hypothesis). However, it is well established that predators also have indirect, sub-lethal effects on their prey where life-history responses to predation risk affect birth and death rates. Here, using a simple model combining cat predation on birds with a sub-lethal (fear) effect of cat density on bird fecundity, we show that these sub-lethal effects may be substantial for urban songbirds. When cat densities are as high as has been recorded in the UK, and even when predation mortality is low (e.g.
Abstract.
2006
Dieng H, Boots M, Tamori N, Higashihara J, Okada T, Kato K, Eshita Y (2006). A35 Adult feeding in the dengue vector Aedes albopictus (Diptera: Culicidae) : male effect and meal status-induced protein expression in the midgut(General presentation,Abstract,The 58th Annual Meeting of the Japan Society of Medical Entomology and Zoology). Medical Entomology and Zoology, 57(Supplement).
Dieng H, Boots M, Tamori N, Higashihara J, Okada T, Kato K, Eshita Y (2006). A37 Embryogenesis in the dengue vector Aedes albopictus (Diptera: Culicidae) : ecological basis and transgenic implications(General presentation,Abstract,The 58th Annual Meeting of the Japan Society of Medical Entomology and Zoology). Medical Entomology and Zoology, 57(Supplement).
Mealor MA, Boots M (2006). An indirect approach to imply trade-off shapes: population level patterns in resistance suggest a decreasingly costly resistance mechanism in a model insect system.
J Evol Biol,
19(2), 326-330.
Abstract:
An indirect approach to imply trade-off shapes: population level patterns in resistance suggest a decreasingly costly resistance mechanism in a model insect system.
Trade-offs between life history and other traits play a key role in shaping the evolution of individuals. It is well established theoretically that the shapes of trade-off curves are as crucial to the evolutionary outcome as their strengths. However, measuring the shape of these relationships directly is often impractical. Here we use an indirect approach that examines the patterns seen within a population and then use theory to infer the shape of the trade-off curve. Using a bioassay we found that most individuals had either high susceptibility or relatively high resistance to a microparasite in a lepidopteran host population. According to general theory, this type of pattern in resistance would be most likely with a deceleratingly costly impact on fitness of increasing resistance. The implications and generality of the approach are discussed, along with the implications of the results to our understanding of the nature of innate resistance to parasites.
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Author URL.
Adams B, Holmes EC, Zhang C, Mammen MP, Nimmannitya S, Kalayanarooj S, Boots M (2006). Cross-protective immunity can account for the alternating epidemic pattern of dengue virus serotypes circulating in Bangkok.
Proc Natl Acad Sci U S A,
103(38), 14234-14239.
Abstract:
Cross-protective immunity can account for the alternating epidemic pattern of dengue virus serotypes circulating in Bangkok.
Dengue virus, the causative agent of dengue fever and its more serious manifestation dengue hemorrhagic fever, is widespread throughout tropical and subtropical regions. The virus exists as four distinct serotypes, all of which have cocirculated in Bangkok for several decades with epidemic outbreaks occurring every 8-10 years. We analyze time-series data of monthly infection incidence, revealing a distinctive pattern with epidemics of serotypes 1, 2, and 3 occurring at approximately the same time and an isolated epidemic of serotype 4 occurring in the intervening years. Phylogenetic analysis of virus samples collected over the same period shows that clade replacement events are linked to the epidemic cycle and indicates that there is an interserotypic immune reaction. Using an epidemic model with stochastic seasonal forcing showing 8- to 10-year epidemic oscillations, we demonstrate that moderate cross-protective immunity gives rise to persistent out-of-phase oscillations similar to those observed in the data, but that strong or weak cross-protection or cross-enhancement only produces in-phase patterns. This behavior suggests that the epidemic pattern observed in Bangkok is the result of cross-protective immunity and may be significantly altered by changes in the interserotypic immune reaction.
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Author URL.
White A, Greenman JV, Benton TG, Boots M (2006). Evolutionary behaviour in ecological systems with trade-offs and non-equilibrium population dynamics.
Evolutionary Ecology Research,
8(3), 387-398.
Abstract:
Evolutionary behaviour in ecological systems with trade-offs and non-equilibrium population dynamics
Question: Do non-equilibrium (cycles or chaos) population dynamics change evolutionary behaviour when compared with equilibrium dynamics? Mathematical methods: the theory of adaptive dynamics is applied to a discrete ecological model with an explicit trade-off between reproduction and survival. Simulation techniques are compared with the theoretical findings. Key assumptions: Mutations in life-history parameters are assumed to be small. A separation of the ecological and evolutionary time scales is assumed. There is a feedback loop between the environment and its inhabitants. Conclusions: with equilibrium population dynamics the shape of the trade-off can be used to characterize the evolutionary behaviour. Trade-offs with accelerating costs produce a continuously stable strategy (CSS). Trade-offs with decelerating costs produce a non-evolutionarily stable strategy (non-ESS) repellor. The characterization holds for non-equilibrium dynamics with low amplitude population oscillations. When the magnitude of the population oscillation exceeds a threshold, the characterization fails. Trade-offs with decelerating costs can produce a CSS, multiple CSSs or evolutionary branching points. The evolution of reproduction and survival parameters may be contingent on initial conditions and sensitive to small changes in other life-history parameters. Evolutionary branching allows types with distinct reproduction and survival parameters to evolve and co-exist. © 2006 Andrew White.
Abstract.
Adams B, Boots M (2006). Modelling the relationship between antibody-dependent enhancement and immunological distance with application to dengue.
J Theor Biol,
242(2), 337-346.
Abstract:
Modelling the relationship between antibody-dependent enhancement and immunological distance with application to dengue.
When antibodies raised in response to a particular pathogen bind with immunologically similar pathogens it may facilitate infection through a phenomenon known as antibody-dependent enhancement (ADE). This process occurs between the four serotypes of dengue virus and, furthermore, secondary infection is a major risk factor in dengue hemorrhagic fever (DHF). Theory has suggested that ADE may be responsible for the large immunological distance between dengue serotypes. We investigate this hypothesis using an epidemic model for dengue in which immunological distance and the strength of immune cross-reaction are expressed separately. Cross-enhancement is considered in three alternative forms acting on susceptibility, transmission and mortality. Previous models have shown that transmission and mortality enhancement can lead to periodicity or chaos. We confirm this result for reasonable levels of susceptibility and transmission enhancement but not for mortality enhancement. We also show that when the two strains have identical basic reproductive numbers no form of enhancement leads to competitive exclusion. When the two strains have different basic reproductive numbers susceptibility or transmission enhancement allow strains with greater immunological similarity to stably coexist but mortality enhancement forces strains to be more distinct. All three forms of enhancement can be associated with DHF and we conclude that mortality enhancement must be dominant if ADE really is responsible for the immunological distance between dengue serotypes.
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Author URL.
Dieng H, Boots M, Tamori N, Higashihara J, Okada T, Kato K, Eshita Y (2006). Some technical and ecological determinants of hatchability in Aedes albopictus, a potential candidate for transposon-mediated transgenesis.
Journal of the American Mosquito Control Association,
22(3), 382-389.
Abstract:
Some technical and ecological determinants of hatchability in Aedes albopictus, a potential candidate for transposon-mediated transgenesis
Fertility is a physiological process of great importance underlying the dynamics of mosquito populations. In transgenesis, it is a prerequisite for the production of subsequent generations and a crucial parameter for evaluating efficiency. Yet, ongoing success in mosquito vector transformation is being severely affected by low embryo survivability. In the prospect of overcoming this impediment, we investigated the darkening/hardening process of the chorion, the effects of some parameters required for transgenesis on hatch success, and erratic hatching in Aedes albopictus, a species that has not yet been targeted for transformation. The eggs from this species, when placed in a moistened environment while whitish, become dark and yet still remain soft approximately 2 h 10 min postoviposition. Those reared in a high moisture environment hatched at a high rate compared with their counterparts submitted to a drier environment. Submission of eggs to p-nitrophenyl-p′-guanidino-benzoate, a substance known to delay the darkening/delay process, resulted in a hatch rate lower than that from eggs soaked in distilled water, which suggests a negative impact on viability. Heat-shock treatment did not taint embryo viability. Overall, eggs displayed a tolerance to an hour of heat shock at 39°C but still hatched at a considerable rate after a 1 hr exposure to 42°C. Hatching was erratic, with a high rate of hatching on the initial flooding and lower rates of hatching on subsequent floodings, all of which resulted cumulatively in considerable hatch success. Our results should serve as a useful reference for the production of both transgenic and laboratory strains of floodwater Aedes mosquitoes. Copyright © 2006 by the American Mosquito Control Association, Inc.
Abstract.
Childs DZ, Cattadori IM, Suwonkerd W, Prajakwong S, Boots M (2006). Spatiotemporal patterns of malaria incidence in northern Thailand.
Trans R Soc Trop Med Hyg,
100(7), 623-631.
Abstract:
Spatiotemporal patterns of malaria incidence in northern Thailand.
We present a detailed analysis of long-term time series of malaria incidence in northern Thailand. Positive cases for Plasmodium falciparum and P. vivax have been recorded monthly from 1977-2002 at 13 provinces in the region. Time series statistical methods are used to examine the long-term trends and seasonal dynamics of malaria incidence at regional and provincial scales. Both malarial types are declining throughout the region, except in the two provinces that share a large border with Myanmar. The rate of decline in P. vivax has decreased across the region since the end of the 1980s, and this may be a signal of developing resistance or changing vector potential. Both species display a two-peak annual seasonality that may be attributed to patterns of vector occurrence, farming practice and migration of individuals across international borders. In a number of provinces, the importance of the first seasonal peak has grown in recent years, possibly owing to increases in vector densities. The medium-term fluctuations of both species exhibit a clear spatial organisation. There is some evidence of a subtle close to 4-year super annual cycle in P. falciparum, which we suggest is driven by extrinsic factors relating to the climate of the region.
Abstract.
Author URL.
Kamo M, Boots M (2006). The evolution of parasite dispersal, transmission, and virulence in spatial host populations.
Evolutionary Ecology Research,
8(7), 1333-1347.
Abstract:
The evolution of parasite dispersal, transmission, and virulence in spatial host populations
Questions: How does parasite dispersal evolve? What is the impact of the evolution of parasite dispersal on the evolution of transmission and virulence? Mathematical methods: Spatially explicit host parasite models with local and global interactions, analysed by pair approximation and simulation. Pairwise invasibility plots. Key assumptions: Infected and susceptible hosts are arranged on a regular lattice. Infection can occur locally or globally with some probability. The proportion of long-distance infection and parasite life-history traits evolve by small mutations between haploid strains. There is no explicit cost to long-distance dispersal. Conclusions: an intermediate degree of long-distance infection always evolves. This is due to a balance between the advantages from long-distance dispersal (avoiding local competition for susceptible hosts) and costs to dispersal (that emerge from the spatial heterogeneity of the hosts). Evolution maximizes parasite transmission rate in a spatially structured host population when parasite dispersal can also evolve. The evolution of parasite dispersal may lead to the concurrent evolution of higher parasite transmission and virulence than found in completely mixed populations. Interactions between the completely local and global are therefore important. © 2006 Masashi Kamo.
Abstract.
Miller MR, White A, Boots M (2006). The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism.
Evolution,
60(5), 945-956.
Abstract:
The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism.
Tolerance to parasites reduces the harm that infection causes the host (virulence). Here we investigate the evolution of parasites in response to host tolerance. We show that parasites may evolve either higher or lower within-host growth rates depending on the nature of the tolerance mechanism. If tolerance reduces virulence by a constant factor, the parasite is always selected to increase its growth rate. Alternatively, if tolerance reduces virulence in a nonlinear manner such that it is less effective at reducing the damage caused by higher growth rates, this may select for faster or slower replicating parasites. If the host is able to completely tolerate pathogen damage up to a certain replication rate, this may result in apparent commensalism, whereby infection causes no apparent virulence but the original evolution of tolerance has been costly. Tolerance tends to increase disease prevalence and may therefore lead to more, rather than less, disease-induced mortality. If the parasite is selected, even a highly efficient tolerance mechanism may result in more individuals in total dying from disease. However, the evolution of tolerance often, although not always, reduces the individual risk of dying from infection.
Abstract.
Author URL.
2005
Ryder JJ, Webberley KM, Boots M, Knell RJ (2005). Measuring the transmission dynamics of a sexually transmitted disease.
Proceedings of the National Academy of Sciences of the United States of America,
102(42), 15140-15143.
Abstract:
Measuring the transmission dynamics of a sexually transmitted disease
Sexually transmitted diseases (STDs) occur throughout the animal kingdom and are generally thought to affect host population dynamics and evolution very differently from other directly transmitted infectious diseases. In particular, STDs are not thought to have threshold densities for persistence or to be able to regulate host population density independently; they may also have the potential to cause host extinction. However, these expectations follow from a theory that assumes that the rate of STD spread depends on the proportion (rather than the density) of individuals infected in a population. We show here that this key assumption ("frequency dependence"), which has not previously been tested in an animal STD system, is invalid in a simple and general experimental model. Transmission of an STD in the two-spot ladybird depended more on the density of infected individuals in the study population than on their frequency. We argue that, in this system, and in many other animal STDs in which population density affects sexual contact rate, population dynamics may exhibit some characteristics that are normally reserved for diseases with density-dependent transmission. © 2005 by the National Academy of Sciences of the USA.
Abstract.
Hamilton R, Boots M, Paterson S (2005). The effect of host heterogeneity and parasite intragenomic interactions on parasite population structure.
Proc Biol Sci,
272(1573), 1647-1653.
Abstract:
The effect of host heterogeneity and parasite intragenomic interactions on parasite population structure.
Understanding the processes that shape the genetic structure of parasite populations and the functional consequences of different parasite genotypes is critical for our ability to predict how an infection can spread through a host population and for the design of effective vaccines to combat infection and disease. Here, we examine how the genetic structure of parasite populations responds to host genetic heterogeneity. We consider the well-characterized molecular specificity of major histocompatibility complex binding of antigenic peptides to derive deterministic and stochastic models. We use these models to ask, firstly, what conditions favour the evolution of generalist parasite genotypes versus specialist parasite genotypes? Secondly, can parasite genotypes coexist in a population? We find that intragenomic interactions between parasite loci encoding antigenic peptides are pivotal in determining the outcome of evolution. Where parasite loci interact synergistically (i.e. the recognition of additional antigenic peptides has a disproportionately large effect on parasite fitness), generalist parasite genotypes are favoured. Where parasite loci act multiplicatively (have independent effects on fitness) or antagonistically (have diminishing effects on parasite fitness), specialist parasite genotypes are favoured. A key finding is that polymorphism is not stable and that, with respect to functionally important antigenic peptides, parasite populations are dominated by a single genotype.
Abstract.
Author URL.
Hamilton R, Boots M, Paterson S (2005). The effect of host heterogeneity and parasite intragenornic interactions on parasite population structure.
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES,
272(1573), 1647-1653.
Author URL.
Miller MR, White A, Boots M (2005). The evolution of host resistance: tolerance and control as distinct strategies.
J Theor Biol,
236(2), 198-207.
Abstract:
The evolution of host resistance: tolerance and control as distinct strategies.
In response to parasitic infection, hosts may evolve defences that reduce the deleterious effects on survivorship. This may be interpreted as a form of resistance, as long as infected hosts are able to either recover or reproduce. Here we distinguish two important routes to this form of resistance. An infected host may either: (1) tolerate pathogen damage, or (2) control the pathogen by inhibiting its growth. A model is constructed to examine the evolutionary dynamics of tolerance and control to a free-living microparasite, where both forms of resistance are costly in terms of other life-history traits. We do not observe polymorphism of tolerant genotypes. In contrast, the evolution of control may lead to disruptive selection, and ultimately dimorphism of extreme strains. The optimal host genotype also varies with the type of resistance-individuals invest more in tolerance and pay a greater cost. The free-living framework used makes the distinction between tolerance and control explicit but the distinction applies equally to directly transmitted parasites. Due to the evolutionary differences exhibited, it is important to design experiments that distinguish between the two forms of resistance.
Abstract.
Author URL.
Greenman JV, Benton TG, Boots M, White AR (2005). The evolution of oscillatory behavior in age-structured species.
Am Nat,
166(1), 68-78.
Abstract:
The evolution of oscillatory behavior in age-structured species.
A major challenge in ecology is to explain why so many species show oscillatory population dynamics and why the oscillations commonly occur with particular periods. The background environment, through noise or seasonality, is one possible driver of these oscillations, as are the components of the trophic web with which the species interacts. However, the oscillation may also be intrinsic, generated by density-dependent effects on the life history. Models of structured single-species systems indicate that a much broader range of oscillatory behavior than that seen in nature is theoretically possible. We test the hypothesis that it is selection that acts to constrain the range of periods. We analyze a nonlinear single-species matrix model with density dependence affecting reproduction and with trade-offs between reproduction and survival. We show that the evolutionarily stable state is oscillatory and has a period roughly twice the time to maturation, in line with observed patterns of periodicity. The robustness of this result to variations in trade-off function and density dependence is tested.
Abstract.
Author URL.
Bowers RG, Hoyle A, White A, Boots M (2005). The geometric theory of adaptive evolution: trade-off and invasion plots.
J Theor Biol,
233(3), 363-377.
Abstract:
The geometric theory of adaptive evolution: trade-off and invasion plots.
The purpose of this paper is to take an entirely geometrical path to determine the evolutionary properties of ecological systems subject to trade-offs. In particular we classify evolutionary singularities in a geometrical fashion. To achieve this, we study trade-off and invasion plots (TIPs) which show graphically the outcome of evolution from the relationship between three curves. The first invasion boundary (curve) has one strain as resident and the other strain as putative invader and the second has the roles of the strains reversed. The parameter values for one strain are used as the origin with those of the second strain varying. The third curve represents the trade-off. All three curves pass through the origin or tip of the TIP. We show that at this point the invasion boundaries are tangential. At a singular TIP, in which the origin is an evolutionary singularity, the invasion boundaries and trade-off curve are all tangential. The curvature of the trade-off curve determines the region in which it enters the singular TIP. Each of these regions has particular evolutionary properties (EUS, CS, SPR and MI). Thus we determine by direct geometric argument conditions for each of these properties in terms of the relative curvatures of the trade-off curve and invasion boundaries. We show that these conditions are equivalent to the standard partial derivative conditions of adaptive dynamics. The significance of our results is that we can determine whether the singular strategy is an attractor, branching point, repellor, etc. simply by observing in which region the trade-off curve enters the singular TIP. In particular we find that, if and only if the TIP has a region of mutual invadability, is it possible for the singular strategy to be a branching point. We illustrate the theory with an example and point the way forward.
Abstract.
Author URL.
2004
Greenman J, Kamo M, Boots M (2004). External forcing of ecological and epidemiological systems: a resonance approach.
Physica D: Nonlinear Phenomena,
190(1-2), 136-151.
Abstract:
External forcing of ecological and epidemiological systems: a resonance approach
Analysing ecological and epidemiological models is complicated by the multiplicity of states that can be excited in the interaction between model nonlinearity and external forcing. This multiplicity, typically created by a hierarchy of subcritical subharmonics, can lead to high amplification of the forcing signal and complex switching under chaos and stochastic externalities. Our objective is to understand the structure of these possible modes of system oscillation, in particular the conditions under which they appear and disappear. The analysis is carried out by transforming the problem into a problem of locating the resonances of the system under variable period forcing. The hierarchy of resonances identified has a well defined generic structure based on the natural period of oscillation of the model, whether stable or unstable when isolated. The usefulness and simplicity of this approach is illustrated in a discussion of a range of human diseases. © 2003 Elsevier B.V. All rights reserved.
Abstract.
Boots M, Hudson PJ, Sasaki A (2004). Large shifts in pathogen virulence relate to host population structure.
Science,
303(5659), 842-844.
Abstract:
Large shifts in pathogen virulence relate to host population structure.
Theory on the evolution of virulence generally predicts selection for an optimal level of virulence determined by trade-offs with transmission and/or recovery. Here we consider the evolution of pathogen virulence in hosts who acquire long-lived immunity and live in a spatially structured population. We show theoretically that large shifts in virulence may occur in pathogen populations as a result of a bistability in evolutionary dynamics caused by the local contact or social population structure of the host. This model provides an explanation for the rapid emergence of the highly virulent strains of rabbit hemorrhagic disease virus.
Abstract.
Author URL.
Boots M (2004). Modelling insect diseases as functional predators.
Author URL.
Boots M (2004). Modelling insect diseases as functional predators.
Physiological Entomology,
29(3 SPEC. ISS.), 237-239.
Abstract:
Modelling insect diseases as functional predators
Many larval diseases of insects allow no recovery once infected. Furthermore, infected individuals are not able to develop into adults and will not therefore reproduce. A simple modelling approach emphasizes the fact that, accordingly, the agents that cause these diseases are functionally predators. It is important to make this distinction and to be cautious in applying inference drawn from models of parasites to these diseases. Sublethal effects are well known in these insect larval diseases, and models show that they have important dynamical implications. Sublethal effects have received less attention in predator-prey interactions, but their functional relationship with insect diseases emphasizes that nonmortality effects of predators may have correspondingly important dynamical implications.
Abstract.
Kamo M, Boots M (2004). The curse of the pharaoh in space: free-living infectious stages and the evolution of virulence in spatially explicit populations.
J Theor Biol,
231(3), 435-441.
Abstract:
The curse of the pharaoh in space: free-living infectious stages and the evolution of virulence in spatially explicit populations.
The idea that parasites with long-lived infective stages may evolve higher virulence has received considerable attention. This idea is called 'the curse of the pharaoh' because of the hypothesis that the death of Lord Carnavon was caused by very long-lived propagules of a highly virulent infectious disease. Here, we examined the evolution of diseases that transmit via free-living stages in a spatial context. We show that, if virulence evolves independently of transmission, long-lived infective stages can select for higher virulence. There is always the evolution of a finite transmission rate, which becomes higher when the infective stages are shorter lived. When a trade-off occurs between transmission and virulence, we show that there is no evidence for the curse of the pharaoh. Indeed, higher transmission and therefore virulence may be selected for by shorter rather than long-lived infective stages.
Abstract.
Author URL.
Boots M, Bowers RG (2004). The evolution of resistance through costly acquired immunity.
Proc Biol Sci,
271(1540), 715-723.
Abstract:
The evolution of resistance through costly acquired immunity.
We examine the evolutionary dynamics of resistance to parasites through acquired immunity. Resistance can be achieved through the innate mechanisms of avoidance of infection and reduced pathogenicity once infected, through recovery from infection and through remaining immune to infection: acquired immunity. We assume that each of these mechanisms is costly to the host and find that the evolutionary dynamics of innate immunity in hosts that also have acquired immunity are quantitatively the same as in hosts that possess only innate immunity. However, compared with resistance through avoidance or recovery, there is less likely to be polymorphism in the length of acquired immunity within populations. Long-lived organisms that can recover at intermediate rates faced with fast-transmitting pathogens that cause intermediate pathogenicity (mortality of infected individuals) are most likely to evolve long-lived acquired immunity. Our work emphasizes that because whether or not acquired immunity is beneficial depends on the characteristics of the disease, organisms may be selected to only develop acquired immunity to some of the diseases that they encounter.
Abstract.
Author URL.
2003
DIENG H, BOOTS M, TUNO N, TSUDA Y, TAKAGI M (2003). 15.Laboratory and field evaluation of Marcocyclops ditinctus, Megacyclops viridis, and Mesocyclops pehpeiensis against the dengue vector Aedes albopictus in a periodomestic area in Nagasaki, Japan. Medical Entomology and Zoology, 54(2).
DIENG H, BOOTS M, TSUDA Y, TAKAGI M (2003). A laboratory oviposition study in Aedes albopictus (Diptera: Culcidae) with reference to habitat size, leaf litter and their interactions. Medical Entomology and Zoology, 54(1), 43-50.
Boots M, Bowers RG (2003). Baseline criteria and the evolution of hosts and parasites: D0, R0 and competition for resources between strains.
J Theor Biol,
223(3), 361-365.
Abstract:
Baseline criteria and the evolution of hosts and parasites: D0, R0 and competition for resources between strains.
Our understanding of the evolution of diseases has been greatly aided by the use of baseline criteria. Here we examine the theoretical and biological relationships of the well known baseline criteria for the evolution of disease (R0) and the recently introduced corresponding criterion for the evolution of resistance in hosts (D0). We show that there is a formal theoretical equivalence between the two criteria and discuss the characteristics of seperability that determine whether the criteria define the course of evolution. These theoretical determinants correspond biologically to whether strains compete for resources or not. We discuss the biological application of the criteria and argue that D0 may be less widely applicable than R0, but does determine the evolution of resistance in populations with fixed carrying capacities.
Abstract.
Author URL.
Tompkins DM, White AR, Boots M (2003). Ecological replacement of native red squirrels by invasive greys driven by disease.
Ecology Letters,
6(3), 189-196.
Abstract:
Ecological replacement of native red squirrels by invasive greys driven by disease
Although a parapoxvirus harmful to red squirrels is present in UK squirrel populations it has not been considered a major cause of red squirrel decline, and replacement by the introduced grey squirrel, mainly because diseased individuals are rarely observed. By developing a generic model we show that parapoxvirus is likely to have played a crucial role in the red squirrel decline even though the prevalence of infection is low. Conservationists are quite rightly concerned with the invasion of exotic organisms such as the grey squirrel. Our work emphasizes that they, along with other ecologists, should pay particular attention to pathogens, even when they occur at low prevalence.
Abstract.
DIENG H, BOOTS M, MWANDAWIRO C, SATHO T, HASEGAWA M, NYAMBURA GJ, SAITA S, KAWADA H, TAUDA Y, TAKAGI M, et al (2003). Effects of a copepod predator on the survivorship and development of Aedes albopictus (Diptera: Culicidae). Medical Entomology and Zoology, 54(2), 187-192.
Bowers RG, White A, Boots M, Geritz SAH, Kisdi E (2003). Evolutionary branching/speciation: Contrasting results from systems with explicit or emergent carrying capacities.
Evolutionary Ecology Research,
5(6), 883-891.
Abstract:
Evolutionary branching/speciation: Contrasting results from systems with explicit or emergent carrying capacities
In this paper, we use the theory of adaptive dynamics to highlight the differences in evolutionary behaviour when contrasting formulations of the carrying capacity are used. We use two predator - prey systems, one with a fixed carrying capacity and one in which the carrying capacity is an emergent property compounded of an intrinsic growth rate and a susceptibility to crowding. We consider prey evolution in both systems and link the evolving parameters by a trade-off which requires that prey with higher per capita growth experience a greater risk of predation. We find that the two approaches for representing the carrying capacity can lead to markedly different evolutionary behaviour. In particular, the possibility of exhibiting evolutionary branching requires an emergent carrying capacity. This is significant, since evolutionary branching is regarded as a possible mechanism by which sympatric speciation may occur.
Abstract.
Wilson K, Knell R, Boots M, Koch-Osborne J (2003). Group living and investment in immune defence: an interspecific analysis.
Journal of Animal Ecology,
72(1), 133-143.
Abstract:
Group living and investment in immune defence: an interspecific analysis
1. Since parasite transmission is often density-dependent, group living is normally thought to lead to an increased exposure to parasitism. As a consequence, it is predicted that animals living in groups will invest more resources (energy, time, risk, etc.) in parasite defence than those living solitarily. 2. We tested this prediction by measuring basal immune parameters in the larvae of 12 species of Lepidoptera, grouped into six phylogenetically matched species-pairs, each comprising one solitary feeding and one gregariously feeding species. 3. Contrary to expectation, the solitary species in all six species-pairs had higher total haemocyte counts than the gregarious species, and in five out of six species-pairs the solitary species also exhibited higher phenoloxidase activity. Both measurements were positively correlated with each other and with the magnitude of the cellular encapsulation response. 4. The relationship between infection risk and group living was investigated with a dynamic, spatially explicit, host-pathogen model. This shows that when individuals aggregate in groups, the per capita risk of infection can be reduced if the lower between-group transmission more than compensates for the higher within-group transmission. 5. We conclude that the expectation that group living always leads to increased exposure to pathogens and parasites is overly simplistic, and that the specific details of the social system in question will determine if there is increased or decreased exposure to infection.
Abstract.
Dieng H, Boots M, Tuno N, Tsuda Y, Takagi M (2003). Life history effects of prey choice by copepods: implications for biocontrol of vector mosquitoes.
J Am Mosq Control Assoc,
19(1), 67-73.
Abstract:
Life history effects of prey choice by copepods: implications for biocontrol of vector mosquitoes.
Macrocyclops distinctus, Megacyclops viridis, and Mesocyclops pehpeiensis, which are common in rice fields during the summer season in Nagasaki, Japan, showed variable potentialities as biological control agents of larval Aedes albopictus, Culex tritaeniorhynchus, and Anopheles minimus in the laboratory. Macrocyclops distinctus and M. viridis, the largest copepod species, had fewer eggs within an egg clutch in nature than the smallest species, M. pehpeiensis, which also had a lower developmental time for sexual maturation (based on the appearance of the 1st clutch). Longevity as well as fecundity were influenced by nutritional conditions and varied significantly between the species. All species had shorter life spans when starved, but resistance to starvation was more pronounced in the larger species. All the species had lower clutch production when starved. Also, although the frequency of clutch production was high in M. pehpeiensis (M. pehpeiensis produced a clutch every 2 days, whereas M. distinctus and M. viridis took on average almost 3 days), total clutch production was far higher in the larger species. The copepods fed readily on mosquito larvae, with M. distinctus and M. viridis killing fewer Ae. albopictus than M. pehpeiensis, which, however, killed fewer An. minimus. These copepods exhibited a similar and limited predation against Cx. tritaeniorhynchus. Results of our study support the contention that these copepods have the potential to be used as biological control agents of immature mosquitoes. Also, our results give useful information on colony maintenance and field introduction. In particular, releasing copepods with Paramecium as food could increase their survival in the habitat of the targeted pest.
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Author URL.
Boots M, Sasaki A (2003). Parasite evolution and extinctions.
Ecology Letters,
6(3), 176-182.
Abstract:
Parasite evolution and extinctions
We examine the evolution of diseases that show the frequency-dependent transmission process that is commonly applied to sexually and vector-transmitted infections. As is commonly found, the basic reproductive ratio (R0) of the parasite is maximized by evolution. This has important implications, as it implies that for a wide range of circumstances diseases that show frequency-dependent transmission may be selected to evolve towards driving their hosts to extinction. This contrasts with the results obtained in spatially explicit models where although parasite-driven host extinction may occur, it is unlikely to evolve. We further show that an evolutionary constraint between transmission and virulence is required for evolution to lead to an endemic coexistence of both the host and the disease. Furthermore, this constraint needs to be saturating, such that transmission is 'bought' at an increasing cost in terms of virulence, to avoid evolution to extinction.
Abstract.
Boots M, Greenman J, Ross D, Norman R, Hails R, Sait S (2003). The population dynamical implications of covert infections in host-microparasite interactions.
Journal of Animal Ecology,
72(6), 1064-1072.
Abstract:
The population dynamical implications of covert infections in host-microparasite interactions
1. The persistence of parasites that are only seen in intermittent outbreaks has intrigued ecologists. Long the subject of speculation, there is now evidence that viral insect diseases can cause covert as well as overt infections. 2. Typically, infection leads to overtly diseased individuals that are infectious and die as a result of the disease, but it can also produce other individuals that show a covert, non-infectious pathology, which is typically asymptomatic. Covertly infected individuals do not die as a result of infection, although they may be affected sublethally such that their reproductive output falls, they may transmit the covert infection vertically and, crucially, they may convert at some rate to overt infectious individuals. In this way the parasites are able to persist in host populations and can be detected only by the use of molecular techniques. 3. Here, we apply novel analytical techniques to a general host-parasite modelling framework and examine the population dynamical consequences of such covert infections. 4. The interplay between various stabilizing and destabilizing forces leads to a highly complex pattern of host dynamics, including a theoretically intriguing pinch point. Covert infections may be stabilizing or destabilizing depending on the specific characteristics of the interaction, particularly in relation to the rate of conversion from covert to overt infection. 5. In general terms, intermediate rates of conversion are stabilizing, while high and low rates may each destabilize the host population. In contrast, there is no consistent pattern for the role of vertical transmission because, in some cases, high levels are stabilizing while in others they are destabilizing. 6. Thus, our results demonstrate that relatively subtle pathogen effects such as covert infections can have important and novel dynamical impacts on the host-pathogen interaction. It also suggests that the effects of covert infection are likely to be systemspecific and information may be required on a system-by-system basis in order to make predictions.
Abstract.
Kawaguchi I, Sasaki A, Boots M (2003). Why are dengue virus serotypes so distantly related? Enhancement and limiting serotype similarity between dengue virus strains.
Proc Biol Sci,
270(1530), 2241-2247.
Abstract:
Why are dengue virus serotypes so distantly related? Enhancement and limiting serotype similarity between dengue virus strains.
Dengue virus, the causative agent of dengue fever, has four major serotypes characterized by large genetic and immunological distances. We propose that the unusually large distances between the serotypes can be explained in the light of a process of antibody-dependent enhancement (ADE) leading to increased mortality. Antibody-dependent enhancement results from a new infection with a particular serotype in an individual with acquired immunity to a different serotype. Classical dengue fever causes negligible mortality, but ADE leads to the risk of developing the significantly more dangerous dengue haemorrhagic fever (DHF) and dengue shock syndrome (DSS). A mathematical model is presented that describes the epidemiological dynamics of two serotypes of a pathogen where there is the possibility of co-infection and reinfection by a different serotype, along with increased mortality as a result of enhancement. We show that if there is no or slightly increased mortality after reinfection (enhancement), serotypes with a small immunological distance can stably coexist. This suggests that a cloud of serotypes with minor serological differences will constitute the viral population. By contrast, if enhancement is sufficiently great, a substantial immunological distance is necessary for two serotypes to stably coexist in the population. Therefore, high mortality owing to enhancement leads to an evolutionarily stable viral community comprising a set of distantly separated serotypes.
Abstract.
Author URL.
2002
Dieng H, Boots M, Tuno N, Tsuda Y, Takagi M (2002). A laboratory and field evaluation of Macrocyclops distinctus, Megacyclops viridis and Mesocyclops pehpeiensis as control agents of the dengue vector Aedes albopictus in a peridomestic area in Nagasaki, Japan.
Med Vet Entomol,
16(3), 285-291.
Abstract:
A laboratory and field evaluation of Macrocyclops distinctus, Megacyclops viridis and Mesocyclops pehpeiensis as control agents of the dengue vector Aedes albopictus in a peridomestic area in Nagasaki, Japan.
The use of the cyclopoid copepods Macrocyclops distinctus (Richard) Megacyclops viridis (Jurine) and Mesocyclops pehpeiensis Hu (Cyclopoida: Cyclopidae) as biological control agents against the dengue vector Aedes albopictus (Skuse) (Diptera: Culicidae) was evaluated. In the laboratory their predatory ability was highest against the younger instars of Ae. albopictus and none of the three copepods killed the fourth instar. Except for M. viridis, predatory ability was affected by the size of the container: the smaller the container, the higher the predation. A 4-month field test was conducted to examine the impact of these predators on wild Ae. albopictus. Thirty artificial containers were placed in a peridomestic area to allow Ae. albopictus colonization. We showed continuous and similar oviposition responses in treated and control containers. The densities of Ae. albopictus showed considerable short-term changes and were much reduced by the copepod species. Macrocyclops and the mixture of all three provided better Ae. albopictus control than either Megacyclops or Mesocyclops alone. When larval densities peaked in the control containers in August and September, the overall reduction due to the copepods was nearly complete. Mesocyclops inoculated alone had the highest population survival. However, the growth and survival of all the copepod species was poor when the three genera were mixed. Based on their performance and survival in the trial, Macrocyclops and Mesocyclops merit consideration as bio-control agents of Ae. albopictus.
Abstract.
Author URL.
Dieng H, Mwandawiro C, Boots M, Morales R, Satho T, Tuno N, Tsuda Y, Takagi M (2002). Leaf litter decay process and the growth performance of Aedes albopictus larvae (Diptera: Culicidae).
J Vector Ecol,
27(1), 31-38.
Abstract:
Leaf litter decay process and the growth performance of Aedes albopictus larvae (Diptera: Culicidae).
Larvae of the mosquito Ae. albopictus typically develop in small aquatic sites such as tree holes and artificial containers. Organic detritus, in particular decaying leaves, is therefore their major carbon source. Here we demonstrate the importance of leaf characteristics, and in particular their rates of decay, in determining the development and survivorship of larvae. We compared the effects of a rapidly decaying leaf, the maple Acer buergerianum (Angiospermae: Aceraceae) and a slowly decaying leaf, the camphor Cinnamomum japonicum (Angiospermae: Lauraceae), on the larval development of Ae. albopictus at different larval densities in laboratory microcosms. Overall, the maple leaves provided a better substrate and the observed growth patterns could be explained on the basis of a difference in nutritive and chemical contents of the two leaf types. At the highest population density, the duration of the larval period was much shorter in maple litter microcosms. Larval mortality gradually increased with population density in the camphor treatment. In contrast in the rapidly decaying leaf litter microcosms, mortality remained low even as densities increased. Mean pupal size was greater in the individuals fed on the rapidly decaying leaf litter as well as at lower density. Size is likely to be correlated with fitness in the field. In general, rapidly decaying leaf litter will favor mosquito growth resulting in quicker development and higher population sizes. This work emphasizes the importance of the local environment on the development of vector mosquitoes and has important implications for control.
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Author URL.
Boots M, Sasaki A (2002). Parasite-driven extinction in spatially explicit host-parasite systems.
Am Nat,
159(6), 706-713.
Abstract:
Parasite-driven extinction in spatially explicit host-parasite systems.
General host-parasite theory suggests that parasites may be implicated in the extinction of their hosts by causing instability that leads to increased risk of stochastic extinction. In contrast, spatially explicit models suggest that the parasite may directly drive the host population to extinction. Here we examine the ecological characteristics of host-parasite interactions that favor parasite-driven host extinction. Pair approximations and simulations show that parasites only drive their hosts to extinction when they significantly reduce host reproduction. As a matter of interest, parasites that have a relatively small effect on host death rate are more likely to cause host extinction. Parasite-driven host extinction occurs at any population size, whereas extinction caused by stochastic effects is less likely to occur in large host populations. Populations may therefore be under threat from parasites that stop host reproduction, and this type of parasite may prove to be the most effective biological pesticide.
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Author URL.
Boots M, Knell RJ (2002). The evolution of risky behaviour in the presence of a sexually transmitted disease.
Proc Biol Sci,
269(1491), 585-589.
Abstract:
The evolution of risky behaviour in the presence of a sexually transmitted disease.
Sexually transmitted diseases (STDs) are widespread in nature, often sterilizing their hosts or causing other pathogenic effects. Despite this, there is a widespread occurrence of behaviours that are likely to increase the risk to an individual of contracting an STD. Here, we examine the evolution of behaviours such as promiscuity or mate choice that increase the risk of contracting an STD, but also provide a fitness benefit. As might be expected, the balance between risk and fitness benefit defines the optimal strategy, but this relationship is not straightforward. In particular, we often predict the coexistence of highly risky and highly risk-averse individuals. Surprisingly, very safe strategists that only suffer a small cost will tend to coexist with highly risky strategists rather than outcompete them as might have been expected. Rather than selecting for monogamy or for reduced mate choice, therefore, the presence of an STD may often lead to variability in either promiscuity or mate choice.
Abstract.
Author URL.
2001
DIENG H, MWANDAWIRO C, BOOTS M, TUNO N, TSUDA Y, TAKAGI M (2001). 10 the importance of leaf litter decay processes to container-breeding mosquito' performance. Medical Entomology and Zoology, 52(2).
2000
Boots M (2000). Density-independent resource limitation and the transmission of an insect pathogen.
Oecologia,
124(2), 172-175.
Abstract:
Density-independent resource limitation and the transmission of an insect pathogen
The effects of resource limitation on the transmission of a pathogen were explored. Resource limitation was achieved by replacing part of the host's diet with an indigestible bulking agent. Populations of the pyrallid moth, Plodia interpunctella, raised on high- and low-quality food regimes were exposed to a granulosis virus. Moths subjected to a lower food quality were more likely to become infected, despite the fact that in previous studies, individuals showed no increased susceptibility when exposed individually to the virus. This effect is suggested to be due to a higher exposure to the pathogen due to a faster feeding rate and longer developmental period. The implications of resource levels to the population dynamics of host-pathogen interactions are discussed.
Abstract.
Mwandawiro C, Boots M, Tuno N, Suwonkerd W, Tsuda Y, Takagi M (2000). Heterogeneity in the host preference of Japanese encephalitis vectors in Chiang Mai, northern Thailand.
Trans R Soc Trop Med Hyg,
94(3), 238-242.
Abstract:
Heterogeneity in the host preference of Japanese encephalitis vectors in Chiang Mai, northern Thailand.
Experiments, using the capture-mark-release-recapture technique inside large nets, were carried out in Chiang Mai, northern Thailand, to examine heterogeneity in the host preference of Japanese encephalitis (JE) vectors. A significantly higher proportion of the vector species that were initially attracted to a cow fed when released into a net with a cow than when released into a net containing a pig. However, Culex vishnui individuals that had been attracted to a pig had a higher feeding rate in a net containing a pig rather than a cow. When mosquitoes were given a choice by being released into a net containing both animals, they exhibited a tendency to feed on the host to which they had originally been attracted. This feeding preference was, however, not shown by the offspring of pig-fed individuals. We have therefore shown evidence of physiological/behavioural conditioning in the host preference of JE vectors rather than genetic variability. Our results suggest that effective control of JE might be achieved by increasing the availability of cows (the dead-end hosts of JE virus) to deflect the vectors from pigs (the amplifying host). The behavioural imprinting which we have found would tend to re-inforce the initial tendency of the vectors to bite cows.
Abstract.
Author URL.
Boots M (2000). Kinship and cannibalism in the Indian meal moth, Plodia interpunctella: No evidence of kin discrimination.
Evolutionary Ecology Research,
2(2), 251-256.
Abstract:
Kinship and cannibalism in the Indian meal moth, Plodia interpunctella: No evidence of kin discrimination
Generally, cannibals should avoid consuming related individuals so as to reduce indirect fitness costs. Here, I examine the effect of kinship on larval cannibalism in the Indian meal moth, Plodia interpunctella. First, a series of 'no-choice' experiments was performed in which third instar larvae were confined with either a second instar sibling or an unrelated second instar individual. Next, 'choice' experiments were performed in which third instar larvae were given the choice of a sibling or an unrelated individual, with all three individuals confined to one petri dish. The results from both experimental designs were consistent in that they showed no evidence that cannibals avoid siblings. Sibling cannibalism occured even when there was a choice of an unrelated individual. It is unclear whether this phenomenon is adaptive.
Abstract.
Boots M, Norman R (2000). Sublethal infection and the population dynamics of host-microparasite interactions.
Journal of Animal Ecology,
69(3), 517-524.
Abstract:
Sublethal infection and the population dynamics of host-microparasite interactions
1. A large group of parasites, including many of the larval pathogens of insects, cause an infection from which infectious hosts are unable to recover. In addition, a proportion of those individuals that do not develop the lethal disease on exposure to the parasite may still be harmed by it. 2. We examined the role of these sublethal effects on host-population dynamics. Specifically we considered the case where there are three distinct classes of individuals: (i) susceptibles; (ii) infected and infectious individuals that will not reproduce and cannot recover; and (iii) sublethally infected individuals. 3. Parasites with sublethal effects are less likely to persist and control their host population. This is a consequence of the sublethally infected individuals not being infective. Less intuitively, the sublethal infection is highly destabilizing, increasing the risk of cyclic behaviour in host-parasite population densities. 4. Because sublethal infection acts as a destabilizing force in these host-parasite interactions, parasites with pronounced sublethal effects may be less effective as classical biological control agents.
Abstract.
Boots M, Sasaki A (2000). The evolutionary dynamics of local infection and global reproduction in host-parasite interactions.
Ecology Letters,
3(3), 181-185.
Abstract:
The evolutionary dynamics of local infection and global reproduction in host-parasite interactions
A fundamental question in both evolutionary biology and parasitology is why do different levels of virulence evolve in different parasites. Here we use explicitly spatial lattice models to show how the spatial relationships of infection and host reproduction determine the degree of virulence that will occur. When the reproduction of the host acts over larger spatial scales than the infection process higher virulence is predicted. In contrast to both the mean-field and the case where infection acts over larger spatial scales than reproduction, the transmission and virulence predicted are always finite as 'self-shading' of infected individuals always occurs. This process may help to explain the evolution of the high virulence of larval diseases of insects where reproduction clearly acts over greater distances than infection.
Abstract.
1999
Boots M, Sasaki A (1999). 'Small worlds' and the evolution of virulence: infection occurs locally and at a distance.
Proc Biol Sci,
266(1432), 1933-1938.
Abstract:
'Small worlds' and the evolution of virulence: infection occurs locally and at a distance.
Why are some discases more virulent than others? Vector-borne diseases such as malaria and water-borne diseases such as cholera are generally more virulent than diseases spread by direct contagion. One factor that characterizes both vector- and water-borne diseases is their ability to spread over long distances, thus causing infection of susceptible individuals distant from the infected individual. Here we show that this ability of the pathogen to infect distant individuals in a spatially structured host population leads to the evolution of a more virulent pathogen. We use a lattice model in which reproduction is local but infection can vary between completely local to completely global. With completely global infection the evolutionarily stable strategy (ESS) is the same as in mean-field models while a lower virulence is predicted as infection becomes more local. There is characteristically a period of relatively moderate increase in virulence followed by a more rapid rise with increasing proportions of global infection as we move beyond a 'critical connectivity'. In the light of recent work emphasizing the existence of 'small world' networks in human populations, our results suggests that if the world is getting 'smaller'--as populations become more connected--diseases may evolve higher virulence.
Abstract.
Author URL.
Boots M (1999). A general host-pathogen model with free-living infective stages and differing rates of uptake of the infective stages by infected and susceptible hosts.
Researches on Population Ecology,
41(2), 189-194.
Abstract:
A general host-pathogen model with free-living infective stages and differing rates of uptake of the infective stages by infected and susceptible hosts
In addition to their lethal effects, pathogens can cause a number of other debilitating effects on infected hosts. A population dynamical model of the interaction between an invertebrate host and a pathogen is constructed to examine the importance of one such debilitating effect on the host population dynamics. Specifically the feeding rate and therefore the uptake of pathogen free-living infective particles by infected individuals is reduced as a consequence of the pathogen infection. The pathogen is more likely to regulate the host and the equilibrium population density of the host is reduced. Less intuitively there is also an increased chance of the pathogen causing cyclic population dynamics in the host.
Abstract.
Boots M, Haraguchi Y (1999). The evolution of costly resistance in host-parasite systems.
American Naturalist,
153(4), 359-370.
Abstract:
The evolution of costly resistance in host-parasite systems
Pairwise invadability analysis is used to examine the evolutionary dynamics of host resistance to microparasitic infection. A continuum of strains of the host differs in susceptibility to infection, with less susceptible strains paying a cost resulting in a lower intrinsic growth rate. With a combination of analytical and graphical pairwise invadability analysis, we show that the evolutionary outcome depends crucially on the shape of the constraint function between resistance and its assumed cost in intrinsic growth rates. When resistance is increasingly costly, a single evolutionarily stable strategy is predicted. Alternatively, with decreasingly costly resistance, we find that the hosts tend to be maximally resistant or not at all resistant. There are conditions under which dimorphism of both these types exists but intermediate resistances do not occur. Independently of the trade-off function used, we are always more likely to get resistant strains of the host when the carrying capacity of the host is high. The pathogenicity of the parasite is also important in determining the likelihood and degree of resistance.
Abstract.
Boots M, Bowers RG (1999). Three mechanisms of host resistance to microparasites-avoidance, recovery and tolerance-show different evolutionary dynamics.
J Theor Biol,
201(1), 13-23.
Abstract:
Three mechanisms of host resistance to microparasites-avoidance, recovery and tolerance-show different evolutionary dynamics.
Parasite resistant hosts may avoid becoming infected, recover more quickly after infection or survive longer once infected. A model is constructed to examine the evolution of costly host resistance to directly transmitted microparasites and these three distinct mechanisms of avoidance, recovery and tolerance are compared. In each case polymorphism is more likely between very dissimilar strains and resistance (by which we mean the resistant strain alone) is always more likely to occur in hosts with high intrinsic productivity. However, the region where polymorphism occurs is relatively much smaller when resistance is through reduced pathogenicity. In particular, polymorphism with highly resistant strains requires correspondingly high costs. This is in contrast to avoidance or recovery resistance, where polymorphism can also occur when high resistance is associated with small costs due to the inability of highly resistant strains with low susceptibility or high recovery to support the parasite alone and hence resist invasion by the susceptible strain. Relatedly, resistance through avoidance and recovery is favoured in response to less pathogenic parasites.
Abstract.
Author URL.
1998
Boots M (1998). Cannibalism and the stage-dependent transmission of a viral pathogen of the Indian meal moth, Plodia interpunctella.
Ecological Entomology,
23(2), 118-122.
Abstract:
Cannibalism and the stage-dependent transmission of a viral pathogen of the Indian meal moth, Plodia interpunctella
1. The transmission of an insect pathogen by cannibalism was studied by a series of choice and no-choice experiments. 2. Infection of Plodia interpunctella larvae with a granulosis virus occurred through cannibalism of infected larvae. 3. Depending on the larval instars of the cannibal and the victim relative to each other, preferential cannibalism of both infected and healthy larvae was observed. 4. Larvae cannibalise healthy, less vulnerable larvae preferentially, but it is argued that there is no evidence that they are avoiding infection. 5. The victim cannibalised can be explained as a balance between the reduced risk of injury and the ease of cannibalism of moribund infected individuals on the one hand and the greater food resource value of healthy individuals on the other. 6. The implications for the insect population dynamics of the transmission of the pathogen via cannibalism and the effective removal of infective particles through cannibalism by immune stages are discussed.
Abstract.
1995
Begon M, Boots M (1995). Covert infection or, simply, resistance?. Functional Ecology, 9(3), 549-550.
Boots M, Begon M (1995). Strain differences in the indian meal moth, Plodia interpunctella, in response to a granulosis virus.
Researches on Population Ecology,
37(1), 37-42.
Abstract:
Strain differences in the indian meal moth, Plodia interpunctella, in response to a granulosis virus
Three strains of the Indian Meal Moth, Plodia interpunctella, were compared in terms of their response to a granulosis virus under different environmental conditions. A significant difference in the relative susceptibilities to the virus of the three laboratory strains was established. Evidence of potential trade-offs with resistance was found in overall fecundity, pupal size and mortality at adult emergence. There was however little evidence that a reduction in resource level led to more trade-offs being apparent. No clear relationship was found between resistance to the lethal effects of the virus and susceptibility to the sublethal effects of the virus. © 1995 Society of Population Ecology.
Abstract.
1994
Bowers RG, Boots M, Begon M (1994). Life-history trade-offs and the evolution of pathogen resistance: competition between host strains.
Proc Biol Sci,
257(1350), 247-253.
Abstract:
Life-history trade-offs and the evolution of pathogen resistance: competition between host strains.
The dynamics of a 'resistant' and a 'susceptible' strain of a self-regulated host species, in the presence of a directly transmitted pathogen, is investigated. The two strains trade off differences in pathogen transmissibility (as an aspect of pathogen resistance) against differences in birth rate and/or resistance to crowding. Depending on parameter values, either strain may be eliminated, or the two may coexist (along with the pathogen). Coexistence (polymorphism), unsurprisingly, requires an appropriate balance between the different advantages possessed by the two strains. The probability of coexistence through such a balance, however, varies nonlinearly with the degree of difference between the strains: coexistence is least likely between two very similar strains. Resistance is most likely to evolve in hosts with the characteristics of many insect pests. Moreover, with highly pathogenic pathogens, a 'susceptible' strain may exclude a 'resistant' strain because its higher growth rate is more effective against the pathogen than reduced transmissibility. 'Resistance' can reside in parameters other than those directly associated with the pathogen. Although no cycles arise and no chaotic behaviour is found, an oscillatory approach to equilibrium is commonly observed, signalling the possibility of observable oscillations in strain frequency in the (more variable) real world.
Abstract.
Author URL.
BOOTS M, BEGON M (1994). Resource limitation and the lethal and sublethal effects of a viral pathogen in the Indian meal moth, Plodia interpunctella.
Ecological Entomology,
19(4), 319-326.
Abstract:
Resource limitation and the lethal and sublethal effects of a viral pathogen in the Indian meal moth, Plodia interpunctella
Abstract. The effects of resource limitation and the lethal and sublethal effects of a granulosis virus on a lepidopteran host, the Indian meal moth, Plodia interpunctella, were examined. The food quality was manipulated by the addition of an inert bulking agent (methyl cellulose) which caused the size, development rate and fecundity of the moths to be reduced. The resource quality had no effect on the mortality due to the virus. In contrast, sublethal effects of the virus on pupal weight were more apparent under conditions of resource limitation. Considerable variation between the sublethal effects after challenge with different doses of the virus was found. The balance between deleterious sublethal effects of the virus and the selection of more robust individuals by the bioassays is proposed as a mechanism to explain this variation. Implications for the dynamics of insect hosts and their pathogens are discussed. Copyright © 1994, Wiley Blackwell. All rights reserved
Abstract.
1993
Boots M, Begon M (1993). Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology, 7(5), 528-534.
