Publications by year
In Press
Lynton-Jenkins J, Brundl A, Cauchoix M, Lejeune L, Salle L, Thiney A, Russell A, Chaine A, Bonneaud C (In Press). Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co-occurring host species. Ecology and Evolution
Bonneaud C, Herrel A, Videlier M (In Press). Intra-individual variation in exploration behaviour in a largely aquatic frog: effects of sex and personality traits. Herpetological Journal
Dowling A, Hill G, Bonneaud C (In Press). Multiple differences in pathogen-host cell interactions following a bacterial host shift. Scientific Reports
Bonneaud C, Giraudeau M, Tardy L, Staley M, Hill GE, McGraw KJ (In Press). Rapid antagonistic coevolution in an emerging pathogen and its vertebrate host. Current Biology, 1-25.
Dobreva MP, Lynton-Jenkins JG, Chaves JA, Tokita M, Bonneaud C, Abzhanov A (In Press). Sex identification in embryos and adults of Darwin’s finches.
Abstract:
Sex identification in embryos and adults of Darwin’s finches
AbstractDarwin’s finches, endemic to the Galapagos and Cocos islands, are an iconic example of adaptive radiation and evolution under natural selection. Comparative genetic studies using embryos of Darwin’s finches have shed light on the possible evolutionary processes underlying the speciation of this clade. Molecular identification of the sex of embryonic samples is important for such studies, where this information often cannot be inferred otherwise. We tested a fast and simple chicken embryo protocol for extraction of genomic DNA on Darwin’s finch embryos. In addition, we suggest modifications to two of the previously reported PCR primer sets for CHD1, a gene used for sexing in adult passerine birds. The sex of all 29 tested embryos of six species of Darwin’s finches was determined successfully by PCR, using both primer sets. Hatchlings/nestlings and fledglings are also impossible to distinguish visually. This includes juveniles of sexually dimorphic species which are yet to moult in adult-like plumage and beak colouration. Furthermore, four species of Darwin’s finches are monomorphic, males and females looking alike. Therefore, sex assessment in the field can be a source of error, especially with respect to juveniles and mature monomorphic birds outside of the mating season. We caught 567 juveniles and adults belonging to six species of Darwin’s finches and only 44% had unambiguous sex-specific morphology. We sexed 363 birds by PCR, including individuals sexed based on marginal sex specific morphological traits (N=278) and birds which were impossible to classify in the field (N=39). For birds with marginal sex specific traits, PCR results revealed a 13% sexing error rate. This demonstrates that PCR based sexing can improve field studies on Darwin’s finches, especially when individuals with unclear sex-related morphology are involved. The protocols used here provide an easy and reliable way to sex Darwin’s finches throughout ontogeny, from embryos to adults.
Abstract.
Bonneaud C, Lucy W, Bram K (In Press). Understanding the emergence of bacterial pathogens in novel hosts. Philosophical Transactions B: Biological Sciences
2023
Ferraguti M, Magallanes S, Jiménez‐Peñuela J, Martínez‐de la Puente J, Garcia‐Longoria L, Figuerola J, Muriel J, Albayrak T, Bensch S, Bonneaud C, et al (2023). Environmental, geographical and time‐related impacts on avian malaria infections in native and introduced populations of house sparrows (. <i>Passer domesticus</i>. ), a globally invasive species. Global Ecology and Biogeography, 32(5), 809-823.
Lynton‐Jenkins JG, Chaine AS, Russell AF, Bonneaud C (2023). Parasite detection and quantification in avian blood is dependent on storage medium and duration. Ecology and Evolution, 13(2).
2021
Lynton-Jenkins JG, Russell AF, Chaves J, Bonneaud C (2021). Avian disease surveillance on the island of San Cristobal, Galapagos.
ECOLOGY AND EVOLUTION,
11(24), 18422-18433.
Author URL.
Zhang Y, Hill GE, Ge Z, Park NR, Taylor HA, Andreasen V, Tardy L, Kavazis AN, Bonneaud C, Hood WR, et al (2021). Effects of a Bacterial Infection on Mitochondrial Function and Oxidative Stress in a Songbird.
Physiol Biochem Zool,
94(2), 71-82.
Abstract:
Effects of a Bacterial Infection on Mitochondrial Function and Oxidative Stress in a Songbird.
AbstractAs a major physiological mechanism involved in cellular renewal and repair, immune function is vital to the body's capacity to support tissue maintenance and organismal survival. Because immune defenses can be energetically expensive, the activities of metabolically active organs, such as the liver, are predicted to increase during infection by most pathogens. However, some pathogens are immunosuppressive, which might reduce the metabolic capacities of select organs to suppress immune response. Mycoplasma gallisepticum (MG) is a well-known immunosuppressive bacterium that infects domestic chickens and turkeys as well as songbirds. In the house finch (Haemorhous mexicanus), which is the primary host for MG among songbird species, MG infects both the respiratory system and the conjunctiva of the eye, causing conspicuous swelling. To study the effect of a systemic bacterial infection on cellular respiration and oxidative damage in the house finch, we measured mitochondrial respiration, mitochondrial membrane potential, reactive oxygen species production, and oxidative damage in the livers of house finches that were wild caught and either infected with MG, as indicated by genetic screening for the pathogen, or free of MG infection. We observed that MG-infected house finches showed significantly lower oxidative lipid and protein damage in liver tissue compared with their uninfected counterparts. Moreover, using complex II substrates, we documented a nonsignificant trend for lower state 3 respiration of liver mitochondria in MG-infected house finches compared with uninfected house finches (P=0.07). These results are consistent with the hypothesis that MG suppresses organ function in susceptible hosts.
Abstract.
Author URL.
Gates D, Staley M, Tardy L, Giraudeau M, Hill G, McGraw K, Bonneaud C (2021). Levels of pathogen virulence and host resistance both shape the antibody response to an emerging bacterial disease. Scientific Reports, 11
Dobreva MP, Lynton-Jenkins JG, Chaves JA, Tokita M, Bonneaud C, Abzhanov A (2021). Sex identification in embryos and adults of Darwin’s finches.
PLOS ONE,
16(3), e0237687-e0237687.
Abstract:
Sex identification in embryos and adults of Darwin’s finches
Darwin’s finches are an iconic example of adaptive radiation and evolution under natural selection. Comparative genetic studies using embryos of Darwin’s finches have shed light on the possible evolutionary processes underlying the speciation of this clade. Molecular identification of the sex of embryonic samples is important for such studies, where this information often cannot be inferred otherwise. We tested a fast and simple chicken embryo protocol to extract DNA from Darwin’s finch embryos. In addition, we applied minor modifications to two of the previously reported PCR primer sets for CHD1, a gene used for sexing adult passerine birds. The sex of all 29 tested embryos of six species of Darwin’s finches was determined successfully by PCR, using both primer sets. Next to embryos, hatchlings and fledglings are also impossible to distinguish visually. This extends to juveniles of sexually dimorphic species which are yet to moult in adult-like plumage and beak colouration. Furthermore, four species of Darwin’s finches are monomorphic, males and females looking alike. Therefore, sex assessment in the field can be a source of error, especially with respect to juveniles and mature monomorphic birds outside of the mating season. We caught 567 juveniles and adults belonging to six species of Darwin’s finches and only 44% had unambiguous sex-specific morphology. We sexed 363 birds by PCR: individuals sexed based on marginal sex specific morphological traits; and birds which were impossible to classify in the field. PCR revealed that for birds with marginal sex specific traits, sexing in the field produced a 13% error rate. This demonstrates that PCR based sexing can improve field studies on Darwin’s finches, especially when individuals with unclear sex-related morphology are involved. The protocols used here provide an easy and reliable way to sex Darwin’s finches throughout ontogeny, from embryos to adults.
Abstract.
Marden E, Abbott RJ, Austerlitz F, Ortiz-Barrientos D, Baucom RS, Bongaerts P, Bonin A, Bonneaud C, Browne L, Alex Buerkle C, et al (2021). Sharing and reporting benefits from biodiversity research.
Mol Ecol,
30(5), 1103-1107.
Author URL.
Ducret V, Richards AJ, Videlier M, Scalvenzi T, Moore KA, Paszkiewicz K, Bonneaud C, Pollet N, Herrel A (2021). Transcriptomic analysis of the trade-off between endurance and burst-performance in the frog Xenopus allofraseri.
BMC Genomics,
22(1).
Abstract:
Transcriptomic analysis of the trade-off between endurance and burst-performance in the frog Xenopus allofraseri.
BACKGROUND: Variation in locomotor capacity among animals often reflects adaptations to different environments. Despite evidence that physical performance is heritable, the molecular basis of locomotor performance and performance trade-offs remains poorly understood. In this study we identify the genes, signaling pathways, and regulatory processes possibly responsible for the trade-off between burst performance and endurance observed in Xenopus allofraseri, using a transcriptomic approach. RESULTS: We obtained a total of about 121 million paired-end reads from Illumina RNA sequencing and analyzed 218,541 transcripts obtained from a de novo assembly. We identified 109 transcripts with a significant differential expression between endurant and burst performant individuals (FDR ≤ 0.05 and logFC ≥2), and blast searches resulted in 103 protein-coding genes. We found major differences between endurant and burst-performant individuals in the expression of genes involved in the polymerization and ATPase activity of actin filaments, cellular trafficking, proteoglycans and extracellular proteins secreted, lipid metabolism, mitochondrial activity and regulators of signaling cascades. Remarkably, we revealed transcript isoforms of key genes with functions in metabolism, apoptosis, nuclear export and as a transcriptional corepressor, expressed in either burst-performant or endurant individuals. Lastly, we find two up-regulated transcripts in burst-performant individuals that correspond to the expression of myosin-binding protein C fast-type (mybpc2). This suggests the presence of mybpc2 homoeologs and may have been favored by selection to permit fast and powerful locomotion. CONCLUSION: These results suggest that the differential expression of genes belonging to the pathways of calcium signaling, endoplasmic reticulum stress responses and striated muscle contraction, in addition to the use of alternative splicing and effectors of cellular activity underlie locomotor performance trade-offs. Ultimately, our transcriptomic analysis offers new perspectives for future analyses of the role of single nucleotide variants, homoeology and alternative splicing in the evolution of locomotor performance trade-offs.
Abstract.
Author URL.
2020
Ducret V, Videlier M, Moureaux C, Bonneaud C, Herrel A (2020). Do female frogs have higher resting metabolic rates than males? a case study with. <i>Xenopus allofraseri</i>. Journal of Zoology, 312(4), 221-226.
Bonneaud C, Longdon B (2020). Emerging pathogen evolution. EMBO reports, 21(9).
Bonneaud C, Tardy L, Hill GE, McGraw KJ, Wilson AJ, Giraudeau M (2020). Experimental evidence for stabilizing selection on virulence in a bacterial pathogen.
Evolution Letters,
4(6), 491-501.
Abstract:
Experimental evidence for stabilizing selection on virulence in a bacterial pathogen
Abstract
. The virulence-transmission trade-off hypothesis has provided a dominant theoretical basis for predicting pathogen virulence evolution, but empirical tests are rare, particularly at pathogen emergence. The central prediction of this hypothesis is that pathogen fitness is maximized at intermediate virulence due to a trade-off between infection duration and transmission rate. However, obtaining sufficient numbers of pathogen isolates of contrasting virulence to test the shape of relationships between key pathogen traits, and doing so without the confounds of evolved host protective immunity (as expected at emergence), is challenging. Here, we inoculated 55 isolates of the bacterial pathogen, Mycoplasma gallisepticum, into non-resistant house finches (Haemorhous mexicanus) from populations that have never been exposed to the disease. Isolates were collected over a 20-year period from outbreak in disease-exposed populations of house finches and vary markedly in virulence. We found a positive linear relationship between pathogen virulence and transmission rate to an uninfected sentinel, supporting the core assumption of the trade-off hypothesis. Further, in support of the key prediction, there was no evidence for directional selection on a quantitative proxy of pathogen virulence and, instead, isolates of intermediate virulence were fittest. Surprisingly, however, the positive relationship between virulence and transmission rate was not underpinned by variation in pathogen load or replication rate as is commonly assumed. Our results indicate that selection favors pathogens of intermediate virulence at disease emergence in a novel host species, even when virulence and transmission are not linked to pathogen load.
Abstract.
Tardy L (2020). Understanding the Evolution of Emerging Bacterial Pathogens in Response to Host Resistance.
Abstract:
Understanding the Evolution of Emerging Bacterial Pathogens in Response to Host Resistance
Understanding the evolution of parasites and hosts following a host-shit event is increasingly recognised as being of great importance to public health and the clinical/veterinary sciences in predicting the behaviour and evolutionary consequences of emerging infectious diseases. Microbial pathogenesis and virulence are remarkably complex traits, and only by considering them in the context of their hosts can we begin to unravel key questions as to how and why disease emerges and persists. The period immediately following a host-shift event, where a pathogen circulating in one host species successfully jumps into another is critical – whether such outbreak events “burn out” or become endemic, and what the ramifications of this might be are difficult to model and predict.
That microbial pathogens and their hosts are in a close coevolutionary relationship has been evident since the early days of our understanding of disease, but it is only relatively recently that the ecological, molecular, genomic and bioinformatic tools all required to understand the subject have become widely available and applicable. In the work presented within this thesis, we utilise an exceptionally well monitored and studied novel host-pathogen interaction – that of the avian bacterial pathogen Mycoplasma gallisepticum and its recently infected novel host the House Finch (Haemorhous mexicanus). Approximately 25 years ago this pathogen jumped from its established host in chickens into the wild passerine finch species, triggering an epidemic which has been well monitored from the outset.
We aim to address how host-pathogen coevolution drives particularly the evolution of microbial virulence. Our current understanding of such host-pathogen interactions within an evolutionary context centres around the mathematical and ecological framework of the “Trade-off hypothesis”, but many of the assumptions linking pathogen virulence, transmission and replication have been difficult to test or to integrate with our modern understanding of how microbial virulence is manifested on a molecular level. In exploring these issues throughout this text, we consider that this work has progressed our understanding in this field and goes some way towards this integration of evolutionary theory and more descriptive classical microbiology / molecular biology.
Abstract.
2019
Padilla P, Ducret V, Bonneaud C, Courant J, Herrel A (2019). Acclimation temperature effects on locomotor traits in adult aquatic anurans (X. tropicalis and X. laevis) from different latitudes: possible implications for climate change.
Conserv Physiol,
7(1).
Abstract:
Acclimation temperature effects on locomotor traits in adult aquatic anurans (X. tropicalis and X. laevis) from different latitudes: possible implications for climate change.
Climate change is in part responsible for the 70% decline in amphibian species numbers worldwide. Although temperature is expected to impact whole-organism performance in ectotherms, reversible thermal acclimation has been suggested as a mechanism that may buffer responses to abrupt temperature changes. Here, we test for an effect of acclimation on locomotor performance traits (jump force and stamina) in adults of two predominantly aquatic and closely related frog species from different climatic regions, Xenopus tropicalis (tropical) and Xenopus laevis (temperate). We find significant effects of acclimation temperature on exertion capacity and for jump force in X. tropicalis but no effect of acclimation temperature on burst performance in X. laevis. Our results suggest that the two locomotor performance traits measured are differentially impacted by acclimation temperature in X. tropicalis. Our results further support the hypothesis that lower-latitude ectotherms might have greater acclimation capacity than high-latitude ones. Finally, our results highlight the importance of investigating multiple performance traits when evaluating how animals may cope with changes in temperature. Further work is required to evaluate the potential for acclimation in mitigating the negative impacts of climate change on amphibian populations.
Abstract.
Author URL.
Tardy L, Giraudeau M, Hill GE, McGraw KJ, Bonneaud C (2019). Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen.
Proc Natl Acad Sci U S A,
116(34), 16927-16932.
Abstract:
Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen.
Host resistance through immune clearance is predicted to favor pathogens that are able to transmit faster and are hence more virulent. Increasing pathogen virulence is, in turn, typically assumed to be mediated by increasing replication rates. However, experiments designed to test how pathogen virulence and replication rates evolve in response to increasing host resistance, as well as the relationship between the two, are rare and lacking for naturally evolving host-pathogen interactions. We inoculated 55 isolates of Mycoplasma gallisepticum, collected over 20 y from outbreak, into house finches (Haemorhous mexicanus) from disease-unexposed populations, which have not evolved protective immunity to M. gallisepticum We show using 3 different metrics of virulence (body mass loss, symptom severity, and putative mortality rate) that virulence has increased linearly over >150,000 bacterial generations since outbreak (1994 to 2015). By contrast, while replication rates increased from outbreak to the initial spread of resistance (1994 to 2004), no further increases have occurred subsequently (2007 to 2015). Finally, as a consequence, we found that any potential mediating effect of replication rate on virulence evolution was restricted to the period when host resistance was initially increasing in the population. Taken together, our results show that pathogen virulence and replication rates can evolve independently, particularly after the initial spread of host resistance. We hypothesize that the evolution of pathogen virulence can be driven primarily by processes such as immune manipulation after resistance spreads in host populations.
Abstract.
Author URL.
Zhang Y, Hill GE, Ge Z, Park N, Taylor H, Andreasen V, Kavazis AN, Bonneaud C, Hood WR (2019). Effects of Mycoplasma gallisepticum on mitochondrial function and oxidative stress in house finch.
Author URL.
Bonneaud C, Tardy L, Giraudeau M, Hill GE, McGraw KJ, Wilson AJ (2019). Evolution of both host resistance and tolerance to an emerging bacterial pathogen.
EVOLUTION LETTERS,
3(5), 544-554.
Author URL.
Giraudeau M, Heidinger B, Bonneaud C, Sepp T (2019). Telomere shortening as a mechanism of long-term cost of infectious diseases in natural animal populations.
Biol Lett,
15(5).
Abstract:
Telomere shortening as a mechanism of long-term cost of infectious diseases in natural animal populations.
Pathogens are potent selective forces that can reduce the fitness of their hosts. While studies of the short-term energetic costs of infections are accumulating, the long-term costs have only just started to be investigated. Such delayed costs may, at least in part, be mediated by telomere erosion. This hypothesis is supported by experimental investigations conducted on laboratory animals which show that infection accelerates telomere erosion in immune cells. However, the generalizability of such findings to natural animal populations and to humans remains debatable. First, laboratory animals typically display long telomeres relative to their wild counterparts. Second, unlike humans and most wild animals, laboratory small-bodied mammals are capable of telomerase-based telomere maintenance throughout life. Third, the effect of infections on telomere shortening and ageing has only been studied using single pathogen infections, yet hosts are often simultaneously confronted with a range of pathogens in the wild. Thus, the cost of an infection in terms of telomere-shortening-related ageing in natural animal populations is likely to be strongly underestimated. Here, we discuss how investigations into the links between infection, immune response and tissue ageing are now required to improve our understanding of the long-term impact of disease.
Abstract.
Author URL.
2018
Staley M, Hill GE, Josefson CC, Armbruster JW, Bonneaud C (2018). Bacterial Pathogen Emergence Requires More than Direct Contact with a Novel Passerine Host.
Infect Immun,
86(3).
Abstract:
Bacterial Pathogen Emergence Requires More than Direct Contact with a Novel Passerine Host.
While direct contact may sometimes be sufficient to allow a pathogen to jump into a new host species, in other cases, fortuitously adaptive mutations that arise in the original donor host are also necessary. Viruses have been the focus of most host shift studies, so less is known about the importance of ecological versus evolutionary processes to successful bacterial host shifts. Here we tested whether direct contact with the novel host was sufficient to enable the mid-1990s jump of the bacterium Mycoplasma gallisepticum from domestic poultry to house finches (Haemorhous mexicanus). We experimentally inoculated house finches with two genetically distinct M. gallisepticum strains obtained either from poultry (Rlow) or from house finches (HF1995) during an epizootic outbreak. All 15 house finches inoculated with HF1995 became infected, whereas Rlow successfully infected 12 of 15 (80%) inoculated house finches. Comparisons among infected birds showed that, relative to HF1995, Rlow achieved substantially lower bacterial loads in the host respiratory mucosa and was cleared faster. Furthermore, Rlow-infected finches were less likely to develop clinical symptoms than HF1995-infected birds and, when they did, displayed milder conjunctivitis. The lower infection success of Rlow relative to HF1995 was not, however, due to a heightened host antibody response to Rlow. Taken together, our results indicate that contact between infected poultry and house finches was not, by itself, sufficient to explain the jump of M. gallisepticum to house finches. Instead, mutations arising in the original poultry host would have been necessary for successful pathogen emergence in the novel finch host.
Abstract.
Author URL.
Staley M, Bonneaud C, McGraw KJ, Vleck CM, Hill GE (2018). Detection of Mycoplasma gallisepticum in House Finches ( Haemorhous mexicanus) from Arizona.
Avian Dis,
62(1), 14-17.
Abstract:
Detection of Mycoplasma gallisepticum in House Finches ( Haemorhous mexicanus) from Arizona.
In 1994, an endemic poultry pathogen, Mycoplasma gallisepticum (MG), was identified as the causative agent of a novel disease in house finches ( Haemorhous mexicanus). After an initial outbreak in Maryland, MG spread rapidly throughout eastern North American populations of house finches. Subsequently, MG spread slowly through the northern interior of North America and then into the Pacific Northwest, finally reaching California in 2006. Until 2009, there were no reports of MG in the southwestern United States east of California. In August 2011, after reports of house finches displaying conjunctivitis characteristic of MG infection in Arizona, we trapped house finches at bird feeders in central Arizona (Tempe) and southern Arizona (Tucson and Green Valley) to assay for MG infection. Upon capture, we noted whether birds exhibited conjunctivitis, and we collected choanal swabs to test for the presence of MG DNA using PCR. We detected MG in finches captured from Green Valley (in ∼12% of birds captured), but not in finches from Tucson or Tempe. Based on resampling of house finches at these sites in July 2014, we suggest that central Arizona finches likely remain unexposed to MG. We also suggest that low urban connectivity between arid habitats of southern and central Arizona or a reduction in the prevalence of MG after its initial arrival in Arizona may be limiting the spread of MG from south to north in Arizona. In addition, the observed conjunctivitis-like signs in house finches that were negative for MG by PCR may be caused primarily by avian pox virus.
Abstract.
Author URL.
Gates DE, Valletta JJ, Bonneaud C, Recker M (2018). Quantitative host resistance drives the evolution of increased virulence in an emerging pathogen.
J Evol Biol,
31(11), 1704-1714.
Abstract:
Quantitative host resistance drives the evolution of increased virulence in an emerging pathogen.
Emergent infectious diseases can have a devastating impact on host populations. The high selective pressures on both the hosts and the pathogens frequently lead to rapid adaptations not only in pathogen virulence but also host resistance following an initial outbreak. However, it is often unclear whether hosts will evolve to avoid infection-associated fitness costs by preventing the establishment of infection (here referred to as qualitative resistance) or by limiting its deleterious effects through immune functioning (here referred to as quantitative resistance). Equally, the evolutionary repercussions these different resistance mechanisms have for the pathogen are often unknown. Here, we investigate the co-evolutionary dynamics of pathogen virulence and host resistance following the epizootic outbreak of the highly pathogenic bacterium Mycoplasma gallisepticum in North American house finches (Haemorhous mexicanus). Using an evolutionary modelling approach and with a specific emphasis on the evolved resistance trait, we demonstrate that the rapid increase in the frequency of resistant birds following the outbreak is indicative of strong selection pressure to reduce infection-associated mortality. This, in turn, created the ecological conditions that selected for increased bacterial virulence. Our results thus suggest that quantitative host resistance was the key factor underlying the evolutionary interactions in this natural host-pathogen system.
Abstract.
Author URL.
2017
Bonneaud C, Staley M, McGraw K, Vleck C, Hill G (2017). Detection of Mycoplasma gallisepticum in House Finches (Haemorhous mexicanus) from Arizona. Avian Diseases
Bonneaud C, Sepil I, Wilfert L, Calsbeek R (2017). Plasmodium Infections in Natural Populations of Anolis sagrei Reflect Tolerance Rather Than Susceptibility. Integrative and Comparative Biology, 57(2), 352-361.
Bonneaud C, Richards A, Herrel A, Seebacher F, Wilson R (2017). Using multi-level transcriptomics and metabolic measures to investigate the trade-off between performance and immunity.
Author URL.
2016
Bonneaud C, Wilson R, Seebacher F (2016). Immune-challenged fish up-regulate their metabolic scope to support locomotion. PLoS One
Staley M, Bonneaud C, Hill GE (2016). Insights into the role of host access in limiting disease emergence in a natural host-pathogen system.
Author URL.
2015
Bonneaud C, Marnocha E, Herrel A, Vanhooydonck B, Irschick DJ, Smith TB (2015). Developmental plasticity affects sexual size dimorphism in an anole lizard. Functional Ecology, 30(2), 235-243.
Staley M, Bonneaud C (2015). Immune responses of wild birds to emerging infectious diseases.
Parasite Immunol,
37(5), 242-254.
Abstract:
Immune responses of wild birds to emerging infectious diseases.
Over the past several decades, outbreaks of emerging infectious diseases (EIDs) in wild birds have attracted worldwide media attention, either because of their extreme virulence or because of alarming spillovers into agricultural animals or humans. The pathogens involved have been found to infect a variety of bird hosts ranging from relatively few species (e.g. Trichomonas gallinae) to hundreds of species (e.g. West Nile Virus). Here we review and contrast the immune responses that wild birds are able to mount against these novel pathogens. We discuss the extent to which these responses are associated with reduced clinical symptoms, pathogen load and mortality, or conversely, how they can be linked to worsened pathology and reduced survival. We then investigate how immune responses to EIDs can evolve over time in response to pathogen-driven selection using the illustrative case study of the epizootic outbreak of Mycoplasma gallisepticum in wild North American house finches (Haemorhous mexicanus). We highlight the need for future work to take advantage of the substantial inter- and intraspecific variation in disease progression and outcome following infections with EID to elucidate the extent to which immune responses confer increased resistance through pathogen clearance or may instead heighten pathogenesis.
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Author URL.
Balenger SL, Bonneaud C, Sefick SA, Edwards SV, Hill GE (2015). Plumage color and pathogen-induced gene expression in a wild bird.
BEHAVIORAL ECOLOGY,
26(4), 1100-1110.
Author URL.
Videlier M, Cornette R, Bonneaud C, Herrel A (2015). Sexual differences in exploration behavior in Xenopus tropicalis?.
J Exp Biol,
218(Pt 11), 1733-1739.
Abstract:
Sexual differences in exploration behavior in Xenopus tropicalis?
The two sexes of a species often differ in many ways. How sexes differ depends on the selective context, with females often investing more in reproductive output and males in territory defense and resource acquisition. This also implies that behavioral strategies may differ between the two sexes, allowing them to optimize their fitness in a given ecological context. Here, we investigated whether males and females differ in their exploration behavior in an aquatic frog (Xenopus tropicalis). Moreover, we explored whether females show different behavioral strategies in the exploration of a novel environment as has been demonstrated previously for males of the same species. Our results show significant sex differences, with males exploring their environment more than females. Yet, similar to males, female exploratory behavior varied significantly among individuals and broadly fell into three categories: shy, intermediate and bold. Moreover, like in males, behavioral strategies are decoupled from morphology and performance. Our results suggest that females are more sedentary than males, with males engaging in greater risk taking by exploring novel environments more. Male and female behaviors could, however, be classified into similar groups, with some individuals being bolder than others and displaying more exploration behavior. The decoupling of morphology and performance from behavior appears to be a general feature in the species and may allow selection to act on both types of traits independently.
Abstract.
Author URL.
Staley M, Bonneaud C, Giradeau M, Mcgraw KJ, Hill GE (2015). The epidemiology of Mycoplasma gallisepticum infections in Arizona house finches (Haemorhous mexicanus).
Author URL.
Richards AJ, Herrel A, Bonneaud C (2015). htsint: a Python library for sequencing pipelines that combines data through gene set generation.
BMC Bioinformatics,
16Abstract:
htsint: a Python library for sequencing pipelines that combines data through gene set generation.
BACKGROUND: Sequencing technologies provide a wealth of details in terms of genes, expression, splice variants, polymorphisms, and other features. A standard for sequencing analysis pipelines is to put genomic or transcriptomic features into a context of known functional information, but the relationships between ontology terms are often ignored. For RNA-Seq, considering genes and their genetic variants at the group level enables a convenient way to both integrate annotation data and detect small coordinated changes between experimental conditions, a known caveat of gene level analyses. RESULTS: We introduce the high throughput data integration tool, htsint, as an extension to the commonly used gene set enrichment frameworks. The central aim of htsint is to compile annotation information from one or more taxa in order to calculate functional distances among all genes in a specified gene space. Spectral clustering is then used to partition the genes, thereby generating functional modules. The gene space can range from a targeted list of genes, like a specific pathway, all the way to an ensemble of genomes. Given a collection of gene sets and a count matrix of transcriptomic features (e.g. expression, polymorphisms), the gene sets produced by htsint can be tested for 'enrichment' or conditional differences using one of a number of commonly available packages. CONCLUSION: the database and bundled tools to generate functional modules were designed with sequencing pipelines in mind, but the toolkit nature of htsint allows it to also be used in other areas of genomics. The software is freely available as a Python library through GitHub at https://github.com/ajrichards/htsint.
Abstract.
Author URL.
2014
Staley M, Bonneaud C, Hill GE (2014). Are more ornamented birds better at combatting disease? Assessing the links between condition and ornamentation.
Author URL.
Videlier M, Bonneaud C, Cornette R, Herrel A (2014). Exploration syndromes in the frog Xenopus (Silurana) tropicalis: correlations with morphology and performance?.
JOURNAL OF ZOOLOGY,
294(3), 206-213.
Author URL.
Careau V, Biro PA, Bonneaud C, Fokam EB, Herrel A (2014). Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs.
Oecologia,
175(2), 471-480.
Abstract:
Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs.
The importance of studying individual variation in locomotor performance has long been recognized as it may determine the ability of an organism to escape from predators, catch prey or disperse. In ectotherms, locomotor performance is highly influenced by ambient temperature (Ta), yet several studies have showed that individual differences are usually retained across a Ta gradient. Less is known, however, about individual differences in thermal sensitivity of performance, despite the fact that it could represent adaptive sources of phenotypic variation and/or additional substrate for selection to act upon. We quantified swimming and jumping performance in 18 wild-caught tropical clawed frogs (Xenopus tropicalis) across a Ta gradient. Maximum swimming velocity and acceleration were not repeatable and individuals did not differ in how their swimming performance varied across Ta. By contrast, time and distance jumped until exhaustion were repeatable across the Ta gradient, indicating that individuals that perform best at a given Ta also perform best at another Ta. Moreover, thermal sensitivity of jumping endurance significantly differed among individuals, with individuals of high performance at low Ta displaying the highest sensitivity to Ta. Individual differences in terrestrial performance increased with decreasing Ta, which is opposite to results obtained in lizards at the inter-specific and among-individual levels. To verify the generality of these patterns, we need more studies on individual variation in thermal reaction norms for locomotor performance in lizards and frogs.
Abstract.
Author URL.
Herrel A, Vasilopoulou-Kampitsi M, Bonneaud C (2014). Jumping performance in the highly aquatic frog, Xenopus tropicalis: sex-specific relationships between morphology and performance.
PeerJ,
2Abstract:
Jumping performance in the highly aquatic frog, Xenopus tropicalis: sex-specific relationships between morphology and performance.
Frogs are characterized by a morphology that has been suggested to be related to their unique jumping specialization. Yet, the functional demands associated with jumping and swimming may not be that different as suggested by studies with semi-aquatic frogs. Here, we explore whether features previously identified as indicative of good burst swimming performance also predict jumping performance in a highly aquatic frog, Xenopus tropicalis. Moreover, we test whether the morphological determinants of jumping performance are similar in the two sexes and whether jumping performance differs in the two sexes. Finally we test whether jumping capacity is positively associated with burst swimming and terrestrial endurance capacity in both sexes. Our results show sex-specific differences in jumping performance when correcting for differences in body size. Moreover, the features determining jumping performance are different in the two sexes. Finally, the relationships between different performance traits are sex-dependent as well with females, but not males, showing a trade-off between peak jumping force and the time jumped to exhaustion. This suggests that different selective pressures operate on the two sexes, with females being subjected to constraints on locomotion due to their greater body mass and investment in reproductive capacity. In contrast, males appear to invest more in locomotor capacity giving them higher performance for a given body size compared to females.
Abstract.
Author URL.
Herrel A, Videlier M, Cornette R, Bonneaud C (2014). Should I stay or should I go: exploration behavior in the frog Xenopus tropicalis.
Author URL.
2013
Cheatsazan H, de Almedia APLG, Russell AF, Bonneaud C (2013). Experimental evidence for a cost of resistance to the fungal pathogen, Batrachochytrium dendrobatidis, for the palmate newt, Lissotriton helveticus.
BMC Ecol,
13Abstract:
Experimental evidence for a cost of resistance to the fungal pathogen, Batrachochytrium dendrobatidis, for the palmate newt, Lissotriton helveticus.
BACKGROUND: Batrachochytrium dendrobatidis (Bd), the causative agent of chytridiomycosis, is decimating amphibians worldwide. Unsurprisingly, the majority of studies have therefore concentrated on documenting morbidity and mortality of susceptible species and projecting population consequences as a consequence of this emerging infectious disease. Currently, there is a paucity of studies investigating the sub-lethal costs of Bd in apparently asymptomatic species, particularly in controlled experimental conditions. Here we report the consequences of a single dose of B. dendrobatidis zoospores on captive adult palmate newts (Lissotriton helveticus) for morphological and behavioural traits that associate with reproductive success. RESULTS: a single exposure to ~2000 zoospores induced a subclinical Bd infection. One week after inoculation 84% of newts tested positive for Bd, and of those, 98% had apparently lost the infection by the day 30. However, exposed newts suffered significant mass loss compared with control newts, and those experimental newts removing higher levels of Bd lost most mass. We found no evidence to suggest that three secondary sexual characteristics (areas of dorsal crest and rear foot webbing, and length of tail filament) were reduced between experimental versus control newts; in fact, rear foot webbing was 26% more expansive at the end of the experiment in exposed newts. Finally, compared with unexposed controls, exposure to Bd was associated with a 50% earlier initiation of the non-reproductive terrestrial phase. CONCLUSIONS: Our results suggest that Bd has measureable, but sub-lethal effects, on adult palmate newts, at least under the laboratory conditions presented. We conclude that the effects reported are most likely to be mediated through the initiation of costly immune responses and/or tissue repair mechanisms. Although we found no evidence of hastened secondary sexual trait regression, through reducing individual body condition and potentially, breeding season duration, we predict that Bd exposure might have negative impacts on populations of palmate newts through reducing individual reproductive success and adult recruitment.
Abstract.
Author URL.
Richards AJ, Kosinski AS, Bonneaud C, Legrand D, Owzark K (2013). lpEdit: an editor to facilitate reproducible analysis via literate programming. Proceedings of the 9th Python in Science conference, 80-84.
2012
Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, Clarke RH, Pérez-Tris J (2012). Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna.
Ecology Letters,
15(10), 1112-1119.
Abstract:
Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna
Knowledge of the processes favouring the establishment of exotic parasites is poor. Herein, we test the characteristics of successful exotic parasites that have co-established in the remote island archipelago of New Zealand, due to the introduction of numerous avian host species. Our results show that avian malaria parasites (AM; parasites of the genus Plasmodium) that successfully invaded are more globally generalist (both geographically widespread and with a broad taxonomic range of hosts) than AM parasites not co-introduced to New Zealand. Furthermore, the successful AM parasites are presently more prevalent in their native range than AM parasites found in the same native range but not co-introduced to New Zealand. This has resulted in an increased number and greater taxonomic diversity of AM parasites now in New Zealand. © 2012 Blackwell Publishing Ltd/CNRS.
Abstract.
Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, Clarke RH, Pérez-Tris J (2012). Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna.
Ecol Lett,
15(10), 1112-1119.
Abstract:
Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna.
Knowledge of the processes favouring the establishment of exotic parasites is poor. Herein, we test the characteristics of successful exotic parasites that have co-established in the remote island archipelago of New Zealand, due to the introduction of numerous avian host species. Our results show that avian malaria parasites (AM; parasites of the genus Plasmodium) that successfully invaded are more globally generalist (both geographically widespread and with a broad taxonomic range of hosts) than AM parasites not co-introduced to New Zealand. Furthermore, the successful AM parasites are presently more prevalent in their native range than AM parasites found in the same native range but not co-introduced to New Zealand. This has resulted in an increased number and greater taxonomic diversity of AM parasites now in New Zealand.
Abstract.
Author URL.
Bonneaud C, Balenger SL, Hill GE, Russell AF (2012). Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird.
Molecular Ecology,
21(19), 4787-4796.
Abstract:
Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird
Protective immunity is expected to evolve when the costs of mounting an immune response are less than those of harbouring pathogens. Estimating the costs of immunity vs. pathogenesis in natural systems is challenging, however, because they are typically closely linked. Here we attempt to disentangle the relative cost of each using experimental infections in a natural host-parasite system in which hosts (house finches, Carpodacus mexicanus) differ in resistance to a bacterium (Mycoplasma gallisepticum, MG), depending on whether they originate from co-evolved or unexposed populations. Experimental infection with a 2007-strain of MG caused finches from co-evolved populations to lose significantly more mass relative to controls, than those from unexposed populations. In addition, infected co-evolved finches that lost the most mass harboured the least amounts of MG, whereas the reverse was true in finches from unexposed populations. Finally, within co-evolved populations, individuals that displayed transcriptional evidence of higher protective immune activity, as indicated by changes in the expression of candidate immune and immune-related genes in a direction consistent with increased resistance to MG, showed greater mass loss and lower MG load. Thus, mass loss appeared to reflect the costs of immunity vs. pathogenesis in co-evolved and unexposed populations, respectively. Our results suggest that resistance can evolve even when the short-term energetic costs of protective immunity exceed those of pathogenesis, providing the longer-term fitness costs of infection are sufficiently high. © 2012 Blackwell Publishing Ltd.
Abstract.
Bonneaud C, Balenger SL, Hill GE, Russell AF (2012). Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird.
Mol Ecol,
21(19), 4787-4796.
Abstract:
Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird.
Protective immunity is expected to evolve when the costs of mounting an immune response are less than those of harbouring pathogens. Estimating the costs of immunity vs. pathogenesis in natural systems is challenging, however, because they are typically closely linked. Here we attempt to disentangle the relative cost of each using experimental infections in a natural host-parasite system in which hosts (house finches, Carpodacus mexicanus) differ in resistance to a bacterium (Mycoplasma gallisepticum, MG), depending on whether they originate from co-evolved or unexposed populations. Experimental infection with a 2007-strain of MG caused finches from co-evolved populations to lose significantly more mass relative to controls, than those from unexposed populations. In addition, infected co-evolved finches that lost the most mass harboured the least amounts of MG, whereas the reverse was true in finches from unexposed populations. Finally, within co-evolved populations, individuals that displayed transcriptional evidence of higher protective immune activity, as indicated by changes in the expression of candidate immune and immune-related genes in a direction consistent with increased resistance to MG, showed greater mass loss and lower MG load. Thus, mass loss appeared to reflect the costs of immunity vs. pathogenesis in co-evolved and unexposed populations, respectively. Our results suggest that resistance can evolve even when the short-term energetic costs of protective immunity exceed those of pathogenesis, providing the longer-term fitness costs of infection are sufficiently high.
Abstract.
Author URL.
Bonneaud C, Balenger SL, Zhang J, Edwards SV, Hill GE (2012). Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird.
Mol Ecol,
21(11), 2628-2639.
Abstract:
Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird.
Innate immunity is expected to play a primary role in conferring resistance to novel infectious diseases, but few studies have attempted to examine its role in the evolution of resistance to emerging pathogens in wild vertebrate populations. Here, we used experimental infections and cDNA microarrays to examine whether changes in the innate and/or acquired immune responses likely accompanied the emergence of resistance in house finches (Carpodacus mexicanus) in the eastern United States subject to a recent outbreak of conjunctivitis-causing bacterium (Mycoplasma gallisepticum-MG). Three days following experimental infection with MG, we observed differences in the splenic transcriptional responses between house finches from eastern U.S. populations, with a 12-year history of MG exposure, versus western U.S. populations, with no history of exposure to MG. In particular, western birds down-regulated gene expression, while eastern finches showed no expression change relative to controls. Studies involving poultry have shown that MG can manipulate host immunity, and our observations suggest that pathogen manipulation occurred only in finches from the western populations, outside the range of MG. Fourteen days after infection, eastern finches, but not western finches, up-regulated genes associated with acquired immunity (cell-mediated immunity) relative to controls. These observations suggest population differences in the temporal course of the response to infection with MG and imply that innate immune processes were targets of selection in response to MG in the eastern U.S. population.
Abstract.
Author URL.
Herrel A, Gonwouo L, Fokam E, Ngundy W, Bonneaud C (2012). Inter-sexual differences in body shape and locomotor performance in the aquatic frog, Xenopus tropicalis. Journal of Zoology(287), 311-316.
Herrel A, Bonneaud C (2012). Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis.
J Exp Biol,
215(Pt 14), 2465-2470.
Abstract:
Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis.
Amphibians are ideal taxa with which to investigate the effects of climate change on physiology, dispersal capacity and distributional ranges as their physiological performance and fitness is highly dependent on temperature. Moreover, amphibians are among the most endangered vertebrate taxa. Here we use the tropical clawed frog, Xenopus tropicalis, as a model system to explore effects of temperature on locomotor performance. Our analyses show that locomotion is thermally sensitive, as illustrated by significant effects of temperature on terrestrial exertion capacity (time until exhaustion) and aquatic burst speed (maximal burst swimming velocity and maximal burst swimming acceleration capacity). Exertion performance measures had relatively lower temperature optima and narrower performance breadth ranges than measures of burst speed. The narrow 80% performance breadths confirm predictions that animals from stable environments should display high thermal sensitivity and, combined with the divergent temperature optima for exertion capacity and burst speed, underscore the vulnerability of tropical species such as X. tropicalis to even relatively small temperature changes. The temperature sensitivity of locomotor performance traits in X. tropicalis suggests that tropical ectotherms may be impacted by predicted changes in climate.
Abstract.
Author URL.
Herrel A, Bonneaud C (2012). Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis.
J Exp Biol,
215(Pt 17), 3106-3111.
Abstract:
Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis.
Trade-offs are thought to impose barriers to phenotypic diversification and may limit the evolutionary responses of organisms to environmental changes. In particular, locomotor trade-offs between endurance or maximal exertion capacity and burst performance capacity have been observed in some species and may constrain the ability of organisms to disperse. Here, we tested for the presence of locomotor trade-offs between maximal exertion and burst performance capacity in an aquatic frog, the tropical clawed frog (Xenopus tropicalis). Given the importance of overland dispersal for this species, we focused on terrestrial exertion capacity (time and distance jumped until exhaustion) and tested whether it trades-off with aquatic burst performance capacity (maximum instantaneous velocity and acceleration), which is likely to be relevant in the context of predator escape and prey capture. Our data show that in both sexes, individuals with longer hindlimbs display higher endurance. Additionally, in females forelimb length was positively correlated with aquatic burst performance capacity and negatively correlated with terrestrial exertion. Trade-offs between endurance and burst performance capacity were detected, but were significant in males only. Finally, males and females differ in morphology and performance. Our data suggest that trade-offs are not universal and may be driven by sex-dependent selection on locomotor capacity. Moreover, our results suggest that locomotor trade-offs may result in sex-biased dispersal under selection for improved endurance capacity as is expected under habitat fragmentation scenarios.
Abstract.
Author URL.
Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV (2012). Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum.
PLoS Genet,
8(2).
Abstract:
Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum.
Measureable rates of genome evolution are well documented in human pathogens but are less well understood in bacterial pathogens in the wild, particularly during and after host switches. Mycoplasma gallisepticum (MG) is a pathogenic bacterium that has evolved predominantly in poultry and recently jumped to wild house finches (Carpodacus mexicanus), a common North American songbird. For the first time we characterize the genome and measure rates of genome evolution in House Finch isolates of MG, as well as in poultry outgroups. Using whole-genome sequences of 12 House Finch isolates across a 13-year serial sample and an additional four newly sequenced poultry strains, we estimate a nucleotide diversity in House Finch isolates of only ∼2% of ancestral poultry strains and a nucleotide substitution rate of 0.8-1.2×10(-5) per site per year both in poultry and in House Finches, an exceptionally fast rate rivaling some of the highest estimates reported thus far for bacteria. We also found high diversity and complete turnover of CRISPR arrays in poultry MG strains prior to the switch to the House Finch host, but after the invasion of House Finches there is progressive loss of CRISPR repeat diversity, and recruitment of novel CRISPR repeats ceases. Recent (2007) House Finch MG strains retain only ∼50% of the CRISPR repertoire founding (1994-95) strains and have lost the CRISPR-associated genes required for CRISPR function. Our results suggest that genome evolution in bacterial pathogens of wild birds can be extremely rapid and in this case is accompanied by apparent functional loss of CRISPRs.
Abstract.
Author URL.
James RS, Tallis J, Herrel A, Bonneaud C (2012). Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis.
J Exp Biol,
215(Pt 3), 552-558.
Abstract:
Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis.
Environmental temperature varies temporally and spatially and may consequently affect organismal function in complex ways. Effects of temperature are often most pertinent on locomotor performance traits of ectothermic animals. Given the importance of locomotion to mobility and dispersion, variability in temperature may therefore affect the current and future distribution of species. Many previous studies have demonstrated that burst muscle performance changes with temperature. However, less is known about the effects of temperature on sustained skeletal muscle performance. The iliotibialis muscle was isolated from eight male Xenopus tropicalis individuals and subjected to in vitro isometric and work-loop studies at test temperatures of 15, 24, 30 and 32°C. Work-loop power output (average power per cycle) was maximised at each temperature by altering stimulation and strain parameters. A series of 10 work loops was also delivered at each test temperature to quantify endurance performance. Warmer test temperatures tended to increase twitch stress (force normalised to muscle cross-sectional area) and significantly increased tetanic stress. Increased temperature significantly reduced twitch and tetanus activation and relaxation times. Increased temperature also significantly increased both burst muscle power output (cycle average) and sustained (endurance) performance during work loop studies. The increase in burst power output between 15 and 24°C yielded a high Q(10) value of 6.86. Recent studies have demonstrated that the negative effects of inorganic phosphate accumulation during prolonged skeletal muscle performance are reduced with increased temperature, possibly explaining the increases in endurance found with increased test temperature in the present study.
Abstract.
Author URL.
2011
Marzal A, Ricklefs RE, Valkiūnas G, Albayrak T, Arriero E, Bonneaud C, Czirják GA, Ewen J, Hellgren O, Hořáková D, et al (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird.
PLoS One,
6(7).
Abstract:
Diversity, loss, and gain of malaria parasites in a globally invasive bird.
Invasive species can displace natives, and thus identifying the traits that make aliens successful is crucial for predicting and preventing biodiversity loss. Pathogens may play an important role in the invasive process, facilitating colonization of their hosts in new continents and islands. According to the Novel Weapon Hypothesis, colonizers may out-compete local native species by bringing with them novel pathogens to which native species are not adapted. In contrast, the Enemy Release Hypothesis suggests that flourishing colonizers are successful because they have left their pathogens behind. To assess the role of avian malaria and related haemosporidian parasites in the global spread of a common invasive bird, we examined the prevalence and genetic diversity of haemosporidian parasites (order Haemosporida, genera Plasmodium and Haemoproteus) infecting house sparrows (Passer domesticus). We sampled house sparrows (N = 1820) from 58 locations on 6 continents. All the samples were tested using PCR-based methods; blood films from the PCR-positive birds were examined microscopically to identify parasite species. The results show that haemosporidian parasites in the house sparrows' native range are replaced by species from local host-generalist parasite fauna in the alien environments of North and South America. Furthermore, sparrows in colonized regions displayed a lower diversity and prevalence of parasite infections. Because the house sparrow lost its native parasites when colonizing the American continents, the release from these natural enemies may have facilitated its invasion in the last two centuries. Our findings therefore reject the Novel Weapon Hypothesis and are concordant with the Enemy Release Hypothesis.
Abstract.
Author URL.
Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, Russell AF, Smith TB (2011). Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest.
Mol Ecol,
20(5), 1049-1061.
Abstract:
Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest.
Malaria parasites use vertebrate hosts for asexual multiplication and Culicidae mosquitoes for sexual and asexual development, yet the literature on avian malaria remains biased towards examining the asexual stages of the life cycle in birds. To fully understand parasite evolution and mechanism of malaria transmission, knowledge of all three components of the vector-host-parasite system is essential. Little is known about avian parasite-vector associations in African rainforests where numerous species of birds are infected with avian haemosporidians of the genera Plasmodium and Haemoproteus. Here we applied high resolution melt qPCR-based techniques and nested PCR to examine the occurrence and diversity of mitochondrial cytochrome b gene sequences of haemosporidian parasites in wild-caught mosquitoes sampled across 12 sites in Cameroon. In all, 3134 mosquitoes representing 27 species were screened. Mosquitoes belonging to four genera (Aedes, Coquillettidia, Culex and Mansonia) were infected with twenty-two parasite lineages (18 Plasmodium spp. and 4 Haemoproteus spp.). Presence of Plasmodium sporozoites in salivary glands of Coquillettidia aurites further established these mosquitoes as likely vectors. Occurrence of parasite lineages differed significantly among genera, as well as their probability of being infected with malaria across species and sites. Approximately one-third of these lineages were previously detected in other avian host species from the region, indicating that vertebrate host sharing is a common feature and that avian Plasmodium spp. vector breadth does not always accompany vertebrate-host breadth. This study suggests extensive invertebrate host shifts in mosquito-parasite interactions and that avian Plasmodium species are most likely not tightly coevolved with vector species.
Abstract.
Author URL.
Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards SV (2011). Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird.
Proc Natl Acad Sci U S A,
108(19), 7866-7871.
Abstract:
Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird.
Wild organisms are under increasing pressure to adapt rapidly to environmental changes. Predicting the impact of these changes on natural populations requires an understanding of the speed with which adaptive phenotypes can arise and spread, as well as of the underlying mechanisms. However, our understanding of these parameters is poor in natural populations. Here we use experimental and molecular approaches to investigate the recent emergence of resistance in eastern populations of North American house finches (Carpodacus mexicanus) to Mycoplasma galliseptum (MG), a severe conjunctivitis-causing bacterium. Two weeks following an experimental infection that took place in 2007, finches from eastern US populations with a 12-y history of exposure to MG harbored 33% lower MG loads in their conjunctivae than finches from western US populations with no prior exposure to MG. Using a cDNA microarray, we show that this phenotypic difference in resistance was associated with differences in splenic gene expression, with finches from the exposed populations up-regulating immune genes postinfection and those from the unexposed populations generally down-regulating them. The expression response of western US birds to experimental infection in 2007 was more similar to that of the eastern US birds studied in 2000, 7 y earlier in the epizootic, than to that of eastern birds in 2007. These results support the hypothesis that resistance has evolved by natural selection in the exposed populations over the 12 y of the epizootic. We hypothesize that host resistance arose and spread from standing genetic variation in the eastern US and highlight that natural selection can lead to rapid phenotypic evolution in populations when acting on such variation.
Abstract.
Author URL.
Sehgal RNM, Buermann W, Harrigan RJ, Bonneaud C, Loiseau C, Chasar A, Sepil I, Valkiūnas G, Iezhova T, Saatchi S, et al (2011). Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird.
Proc Biol Sci,
278(1708), 1025-1033.
Abstract:
Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird.
Critical to the mitigation of parasitic vector-borne diseases is the development of accurate spatial predictions that integrate environmental conditions conducive to pathogen proliferation. Species of Plasmodium and Trypanosoma readily infect humans, and are also common in birds. Here, we develop predictive spatial models for the prevalence of these blood parasites in the olive sunbird (Cyanomitra olivacea). Since this species exhibits high natural parasite prevalence and occupies diverse habitats in tropical Africa, it represents a distinctive ecological model system for studying vector-borne pathogens. We used PCR and microscopy to screen for haematozoa from 28 sites in Central and West Africa. Species distribution models were constructed to associate ground-based and remotely sensed environmental variables with parasite presence. We then used machine-learning algorithm models to identify relationships between parasite prevalence and environmental predictors. Finally, predictive maps were generated by projecting model outputs to geographically unsampled areas. Results indicate that for Plasmodium spp. the maximum temperature of the warmest month was most important in predicting prevalence. For Trypanosoma spp. seasonal canopy moisture variability was the most important predictor. The models presented here visualize gradients of disease prevalence, identify pathogen hotspots and will be instrumental in studying the effects of ecological change on these and other pathogens.
Abstract.
Author URL.
2009
Bonneaud C, Sinsheimer JS, Richard M, Chastel O, Sorci G (2009). Mhc polymorphisms fail to explain the heritability of phytohaemagglutinin-induced skin swelling in a wild passerine.
Biol Lett,
5(6), 784-787.
Abstract:
Mhc polymorphisms fail to explain the heritability of phytohaemagglutinin-induced skin swelling in a wild passerine.
Genetic estimates of the variability of immune responses are rarely examined in natural populations because of confounding environmental effects. As a result, and because of the difficulty of pinpointing the genetic determinants of immunity, no study has to our knowledge examined the contribution of specific genes to the heritability of an immune response in wild populations. We cross-fostered nestling house sparrows to disrupt the association between genetic and environmental effects and determine the heritability of the response to a classic immunological test, the phytohaemagglutinin (PHA)-induced skin swelling. We detected significant heritability estimates of the response to PHA, of body mass and tarsus length when nestlings were 5 and 10 days old. Variation at Mhc genes, however, did not explain a significant portion of the genetic variation of nestling swelling to PHA. Our results suggest that while PHA-induced swelling is influenced by the nest of origin, the importance of additive genetic variation relative to non-additive genetic variation and the genetic factors that influence the former in wild populations still need to be identified for this trait.
Abstract.
Author URL.
Bonneaud C, Sepil I, Mila B, Buermann W, Pollinger J, Sehgal R, Valkiunas G, Iezhova TA, Saatchi S, Smith TB, et al (2009). The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. Journal of Tropical Ecology(25), 439-447.
2008
Calsbeek R, Bonneaud C, Smith TB (2008). Differential fitness effects of immunocompetence and neighbourhood density in alternative female lizard morphs.
J Anim Ecol,
77(1), 103-109.
Abstract:
Differential fitness effects of immunocompetence and neighbourhood density in alternative female lizard morphs.
1. A growing number of studies demonstrate that natural selection acts on traits important in whole animal performance and physiology. 2. Here we describe a heritable polymorphism in female dorsal pattern in the lizard Anolis sagrei (Dumeril & Bibron 1837). 3. Morphs did not differ in body size or habitat use (perch diameter), however, we show that the social environment, estimated by the number of female neighbours, had different selective effects on alternative morphs in nature. 4. We show that morphs displayed a significantly different immune response to phytohaemagglutinin. Furthermore, natural selection differentially acted on combinations of female morph and immunocompetence, favouring high levels of immune function in one morph and low levels of immune function in the other. 5. We discuss the possibility that morph-specific investments in life-history traits may lead to correlational selection between traits, even when those traits are likely to be determined by different genetic loci.
Abstract.
Author URL.
Bonneaud C, Burnside J, Edwards SV (2008). High-speed developments in avian genomics. Bioscience(58), 587-595.
Calsbeek R, Bonneaud C (2008). Postcopulatory fertilization bias as a form of cryptic sexual selection.
Evolution,
62(5), 1137-1148.
Abstract:
Postcopulatory fertilization bias as a form of cryptic sexual selection.
Males and females share most of their genetic material yet often experience very different selection pressures. Some traits that are adaptive when expressed in males may therefore be maladaptive when expressed in females. Recent studies demonstrating negative correlations in fitness between parents and their opposite-sex progeny suggest that natural selection may favor a reduction in trait correlations between the sexes to partially mitigate intralocus sexual conflict. We studied sex-specific forms of selection acting in Anolis lizards in the Greater Antilles, a group for which the importance of natural selection has been well documented in species-level diversification, but for which less is known about sexual selection. Using the brown anole (Anolis sagrei), we measured fitness-related variation in morphology (body size), and variation in two traits reflecting whole animal physiological condition: running endurance and immune function. Correlations between body size and physiological traits were opposite between males and females and the form of natural selection acting on physiological traits significantly differed between the sexes. Moreover, physiological traits in progeny were correlated with the body-size of their sires, but correlations were null or even negative between parents and their opposite-sex progeny. Although results based on phenotypic and genetic correlations, as well as the action of natural selection, suggest the potential for intralocus sexual conflict, females used sire body size as a cue to sort sperm for the production of either sons or daughters. Our results suggest that intralocus sexual conflict may be at least partly resolved through post-copulatory sperm choice in A. sagrei.
Abstract.
Author URL.
2007
Calsbeek R, Bonneaud C, Pradhu S, Manoukis N, Smith TB (2007). Multiple paternity and sperm storage lead to increased genetic diversity in Anolis lizard. Evolutionary Ecology Research(9), 495-503.
Pérez-Tris J, Hellgren O, Krizanauskiene A, Waldenström J, Secondi J, Bonneaud C, Fjeldså J, Hasselquist D, Bensch S (2007). Within-host speciation of malaria parasites.
PLoS One,
2(2).
Abstract:
Within-host speciation of malaria parasites.
BACKGROUND: Sympatric speciation-the divergence of populations into new species in absence of geographic barriers to hybridization-is the most debated mode of diversification of life forms. Parasitic organisms are prominent models for sympatric speciation, because they may colonise new hosts within the same geographic area and diverge through host specialization. However, it has been argued that this mode of parasite divergence is not strict sympatric speciation, because host shifts likely cause the sudden effective isolation of parasites, particularly if these are transmitted by vectors and therefore cannot select their hosts. Strict sympatric speciation would involve parasite lineages diverging within a single host species, without any population subdivision. METHODOLOGY/PRINCIPAL FINDINGS: Here we report a case of extraordinary divergence of sympatric, ecologically distinct, and reproductively isolated malaria parasites within a single avian host species, which apparently occurred without historical or extant subdivision of parasite or host populations. CONCLUSIONS/SIGNIFICANCE: This discovery of within-host speciation changes our current view on the diversification potential of malaria parasites, because neither geographic isolation of host populations nor colonization of new host species are any longer necessary conditions to the formation of new parasite species.
Abstract.
Author URL.
2006
Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006). Complex Mhc-based mate choice in a wild passerine.
Proc Biol Sci,
273(1590), 1111-1116.
Abstract:
Complex Mhc-based mate choice in a wild passerine.
The extreme polymorphism of the vertebrate major histocompatibility complex (Mhc) is famous for protecting hosts against constantly evolving pathogens. Mate choice is often evoked as a means of maintaining Mhc variability through avoidance of partners with similar Mhc alleles or preference for heterozygotes. Evidence for these two hypotheses mostly comes from studies on humans and laboratory mice. Here, we tested these hypotheses in a wild outbred population of house sparrows (Passer domesticus). Females were not more or less closely related to the males they paired with when considering neutral genetic variation. However, males failed to form breeding pairs when they had too few Mhc alleles and when they were too dissimilar from females at Mhc loci (i.e. had no common alleles). Furthermore, pairs did not form at random as Mhc diversity positively correlated in mating pairs. These results suggest that mate choice evolves in response to (i) benefits in terms of parasite resistance acquired from allelic diversity, and (ii) costs associated with the disruption of co-adapted genes.
Abstract.
Author URL.
Bonneaud C, Perez-Tris J, Federici P, Chastel O, Sorci G (2006). Major histocompatibility alleles associated with local resistance to malaria in a passerine.
EVOLUTION,
60(2), 383-389.
Author URL.
Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G (2006). Major histocompatibility alleles associated with local resistance to malaria in a passerine.
Evolution,
60(2), 383-389.
Abstract:
Major histocompatibility alleles associated with local resistance to malaria in a passerine.
Malaria parasites are a major cause of human mortality in tropical countries and a potential threat for wildlife, as witnessed by the malaria-induced extinction of naive Hawaiian avifauna. Identifying resistance mechanisms is therefore crucial both for human health and wildlife conservation. Patterns of malaria resistance are known to be highly polygenic in both humans and mice, with marked contributions attributed to major histocompatibility (Mhc) genes. Here we show that specific Mhc variants are linked to both increased resistance and susceptibility to malaria infection in a wild passerine species, the house sparrow (Passer domesticus). In addition, links between host immunogenetics and resistance to malaria involved population-specific alleles, suggesting local adaptation in this host-parasite interaction. This is the first evidence for a population-specific genetic control of resistance to malaria in a wild species.
Abstract.
Author URL.
2005
Bonneaud C, Richard M, Faivre B, Westerdahl H, Sorci G (2005). An Mhc class I allele associated to the expression of T-dependent immune response in the house sparrow.
Immunogenetics,
57(10), 782-789.
Abstract:
An Mhc class I allele associated to the expression of T-dependent immune response in the house sparrow.
The major histocompatibility complex (Mhc) encodes for highly variable molecules, responsible for foreign antigen recognition and subsequent activation of immune responses in hosts. Mhc polymorphism should hence be related to pathogen resistance and immune activity, with individuals that carry either a higher diversity of Mhc alleles or one specific Mhc allele exhibiting a stronger immune response to a given antigen. Links between Mhc alleles and immune activity have never been explored in natural populations of vertebrates. To fill this gap, we challenged house sparrows (Passer domesticus) with two T-dependent antigens (phytohemagglutinin and sheep red blood cells) and examined both primary and secondary immune responses in relation to their Mhc class I genotypes. The total number of Mhc alleles had no influence on either primary or secondary response to the two antigens. One particular Mhc allele, however, was associated with an increased response to both antigens. Our results point toward a contribution of the Mhc, or of other genes in linkage disequilibrium with the Mhc, in the regulation of immune responses in a wild animal species.
Abstract.
Author URL.
2004
Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H (2004). Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus).
Immunogenetics,
55(12), 855-865.
Abstract:
Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus).
In order to understand the expression and evolution of host resistance to pathogens, we need to examine the links between genetic variability at the major histocompatibility complex ( Mhc), phenotypic expression of the immune response and parasite resistance in natural populations. To do so, we characterized the Mhc class I and IIB genes of house sparrows with the goal of designing a PCR-based genotyping method for the Mhc genes using denaturing gradient gel electrophoresis (DGGE). The incredible success of house sparrows in colonizing habitats worldwide allows us to assess the importance of the variability of Mhc genes in the face of various pathogenic pressures. Isolation and sequencing of Mhc class I and IIB alleles revealed that house sparrows have fewer loci and fewer alleles than great reed warblers. In addition, the Mhc class I genes divided in two distinct lineages with different levels of polymorphism, possibly indicating different functional roles for each gene family. This organization is reminiscent of the chicken B complex and Rfp-Y system. The house sparrow Mhc hence appears to be intermediate between the great reed warbler and the chicken Mhc, both in terms of numbers of alleles and existence of within-class lineages. We specifically amplified one Mhc class I gene family and ran the PCR products on DGGE gels. The individuals screened displayed between one and ten DGGE bands, indicating that this method can be used in future studies to explore the ecological impacts of Mhc diversity.
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Bonneaud C, Mazuc J, Chastel O, Westerdahl H, Sorci G (2004). Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow.
Evolution,
58(12), 2823-2830.
Abstract:
Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow.
The terminal investment hypothesis predicts that individuals should invest more in their present reproduction if they are less likely to survive to future reproductive events. Infections, which reduce viability, may be used by individuals as a cue of a diminishing residual reproductive value and could therefore theoretically trigger an intensification of breeding effort. We tested this hypothesis in a natural population of house sparrows (Passer domesticus). We manipulated the immune system of breeding females by injecting them with a vaccine against the Paramyxo virus, the agent of Newcastle disease. Females were captured and treated immediately after completion of their first clutch either with the vaccine (NDV) or with phosphate buffered saline (PBS). The entire clutch was subsequently removed. We also screened Mhc class I genes of females to assess possible genotype-by-immune treatment interactions on reproductive investment. Our results indicate that vaccinated females were more likely to lay replacement clutches and that the difference in number of eggs between first and replacement clutches was greater for NDV females than for controls. In addition, chick size, both in terms of tarsus length and body mass, was affected by immune activation but in interaction with nestling age and female body mass, respectively. Mhc genotype-by-immune treatment interactions were never significant; however, allelic diversity was positively correlated with nestling survival. These results show that immune system activation is potentially used as a cue of reduced survival prospect and appears to induce a costly terminal investment behavior, and Mhc diversity might be under selection in a natural population of house sparrows.
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2003
Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003). Assessing the cost of mounting an immune response.
Am Nat,
161(3), 367-379.
Abstract:
Assessing the cost of mounting an immune response.
The evolution of parasite resistance has often been assumed to be governed by antagonistic selection pressures. Defense against pathogens, by mounting an immune response, confers evident benefits but may also incur costs, so that the optimal level of defense is expected to depend on the balance between benefits and costs. Although the benefits of immune surveillance are well known, estimates of costs are still equivocal. Here we studied the behavioral and physiological modifications associated with exposure to a nonreplicating antigen (lipopolysaccharide [LPS] of Escherichia coli) in a passerine species, the house sparrow (Passer domesticus). We further investigated whether the behavioral and physiological changes provoked by LPS induced measurable repercussions on life-history traits, such as the breeding effort and reproductive success. Finally, we tested whether the trade-off between immune activation and breeding effort was modulated by the workload required to feed the brood. Exposure to LPS reduced activity and increased body mass loss of captive individuals; similarly, LPS injection induced a dramatic drop in feeding rate and reproductive success of breeding females. However, this reduction depended on brood size, suggesting that the strength of the trade-off between immune activation and reproduction was affected by the workload required to feed the brood. Overall, this study stresses the magnitude of costs associated with mounting immune responses and the ecological and evolutionary consequences for natural populations.
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Mazuc J, Bonneaud C, Chastel O, Sorci G (2003). Maternal testosterone in eggs and social context in the house sparrow (Passer domesticus). Ecology Letters(6), 1084-1090.
Mazuc J, Bonneaud C, Chastel O, Sorci G (2003). Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus).
ECOLOGY LETTERS,
6(12), 1084-1090.
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