Publications by year
2023
Hansford KM, Gillingham EL, Vaux AGC, Cull B, McGinley L, Catton M, Wheeler BW, Tschirren B, Medlock JM (2023). Impact of green space connectivity on urban tick presence, density and Borrelia infected ticks in different habitats and seasons in three cities in southern England. Ticks and Tick-borne Diseases, 14(2), 102103-102103.
Romero-Haro AÁ, Pérez-Rodríguez L, Tschirren B (2023). Increased male-induced harm in response to female-limited selection: interactive effects between intra- and interlocus sexual conflict?.
Proceedings of the Royal Society B: Biological Sciences,
290(1997).
Abstract:
Increased male-induced harm in response to female-limited selection: interactive effects between intra- and interlocus sexual conflict?
. Interlocus sexual conflict (IRSC) occurs because of shared interactions that have opposite effects on male and female fitness. Typically, it is assumed that loci involved in IRSC have sex-limited expression and are thus not directly affected by selective pressures acting on the other sex. However, if loci involved in IRSC have pleiotropic effects in the other sex, intersexual selection can shape the evolutionary dynamics of conflict escalation and resolution, as well as the evolution of reproductive traits linked to IRSC loci, and vice versa. Here we used an artificial selection approach in Japanese quail (
. Coturnix japonica
. ) to test if female-limited selection on reproductive investment affects the amount of harm caused by males during mating. We found that males originating from lines selected for high female reproductive investment caused more oxidative damage in the female reproductive tract than males originating from lines selected for low female reproductive investment. This male-induced damage was specific to the oviduct and not found in other female tissues, suggesting that it was ejaculate-mediated. Our results suggest that intersexual selection shapes the evolution of IRSC and that male-induced harm may contribute to the maintenance of variation in female reproductive investment.
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Hansford KM, McGinley L, Wheeler BW, Tschirren B, Medlock JM (2023). Ixodes ricinus density, Borrelia prevalence and the density of infected nymphs along an urban-rural gradient in southern England.
Zoonoses Public Health,
70(4), 304-314.
Abstract:
Ixodes ricinus density, Borrelia prevalence and the density of infected nymphs along an urban-rural gradient in southern England.
Ticks are found across a range of habitats, with woodland being particularly important for high densities and prevalence of Borrelia infection. Assessments of risk in urban woodland can be difficult if there are low densities and small sample sizes for Borrelia prevalence estimates. This study targeted six urban woodlands with established tick populations, as well as six woodlands in peri-urban zones and six woodlands in rural zones in and around the cities of Bath and Southampton, in the South of England. Nymph densities were estimated, and 100 nymphs were tested from each of the 18 woodlands studied. Ixodes ricinus ticks were found in all woodlands surveyed, and overall density of nymphs (DON) per 100 m2 was 18.17 in urban woodlands, 26.0 in peri-urban woodlands and 17.67 in rural woodlands. Out of 600 nymphs tested across urban woodlands, 10.3% were infected with Borrelia. The same proportion of nymphs collected in rural woodlands were positive for Borrelia. In peri-urban woodlands, 10.8% of nymphs tested positive. Across both cities combined, density of infected nymphs (DIN) was 2.73 per 100 m2 in peri-urban woodland, 1.87 per 100 m2 in urban woodland and 1.82 per 100 m2 in rural woodland. Overall, DON, Borrelia prevalence and DIN did not differ significantly along an urban-rural gradient. This suggests the risk of Lyme borreliosis transmission could be similar, or perhaps even elevated in urban woodland if there is higher public footfall, subsequent contact with ticks and less awareness of the risks. This is particularly important from a public health perspective, as Borrelia garinii dominated across the gradient and this genospecies is linked to neuroborreliosis.
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Vedder O, Tschirren B, Postma E, Moiron M (2023). Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.
Evolution,
77(11), 2484-2491.
Abstract:
Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.
Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments.
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2022
Hansford K (2022). Ecology and Public Health Risk of Ixodes ricinus (Acari: Ixodidae) in Urban Green Space.
Abstract:
Ecology and Public Health Risk of Ixodes ricinus (Acari: Ixodidae) in Urban Green Space.
Lyme borreliosis is the most common tick-borne disease reported across Europe and North America. Intrinsically linked to the distribution of key tick vector species, it is important to better understand ecological factors that may result in changes in tick distribution and the potential impact this may have on tick-borne disease risk.
The main objective of this thesis was to better determine the spatial distribution of questing Ixodes ricinus across urban landscapes and to investigate site level and landscape level factors that have a significant influence on Lyme borreliosis risk. A multidisciplinary approach, using literature, field, and laboratory-based research, as well as geospatial datasets, was used to investigate and highlight the potential risk posed by urban Lyme borreliosis transmission cycles.
Four studies were completed, the first (Chapter 3) being a review of questing I. ricinus data published from studies in urban areas across Europe over the last 32 years. Three other studies were conducted, centred around questing tick presence, nymph density, Borrelia prevalence and the density of infected nymphs (Lyme borreliosis risk indicators). One investigated the effect of habitat in and around the city of Bath in 2015 and 2016 (Chapter 4). Another investigated local and wider habitat and connectivity factors in Bath, Bristol, and Southampton in 2017 (Chapter 5). The final study incorporated data along an urban-rural gradient in the cities of Bath and Southampton in 2018 (Chapter 6).
Key findings from this thesis were evidence of the presence of I. ricinus infected with Borrelia in a wide range of urban green spaces across Europe (Chapter 3), confirming the potential for contact and possible subsequent transmission of Lyme borreliosis to humans. Tick presence and nymph density were significantly higher in woodland compared to other urban green space habitats (Chapters 4 and 5), and better connectivity to woodland had a similar significant effect (Chapter 5). A seasonal pattern in questing I. ricinus activity was observed in urban green space, with density being significantly higher in spring and summer (Chapter 5). Woodlands across an urban-rural gradient supported similar nymph densities and Borrelia prevalence (Chapter 6), suggesting risk to public health could be similar, or perhaps elevated in urban woodland where potential for human-tick contact could be higher. This could be worsened by the dominance of Borrelia garinii detected in questing I. ricinus in urban green space (Chapters 4, 5 and 6), as this genospecies is linked to neuroborreliosis. Overall, the density of infected nymphs, a key Lyme borreliosis risk indicator, was low (Chapters 4, 5 and 6) compared to other studies in southern England, and indeed the average across Europe (Chapter 3). Key questions remain, however, around the risk of urban woodlands for Lyme borreliosis transmission due to high numbers of visitors.
This thesis presents Lyme borreliosis risk indicators for urban green space, synthesising European and country-level estimates from existing studies and generating new data for southern England. This contributes to the growing evidence of potential risk posed by Borrelia infected ticks in urban areas, which requires further consideration by scientists, policy makers and public health professionals alike. This is particularly crucial as urbanisation and urban greening accelerate, bringing members of the public into proximity with infected ticks, potentially increasing the risk of Lyme borreliosis transmission.
Abstract.
Mitchell C (2022). Evolutionary and ecological immunology of. Toll-like receptors in mammals: patterns of selection within and across taxa.
Abstract:
Evolutionary and ecological immunology of. Toll-like receptors in mammals: patterns of selection within and across taxa
Infection from pathogens is consequential in host survival and fitness. Genetic differences in immune components can provide benefits in defending a host from pathogens. The Toll-like receptors (TLRs) are a family on innate immune receptors which detect pathogen components and have been found to show signs of positive selection across taxa. Genetic variation within TLRs has also been shown to relate to susceptibility to infection. In the first chapter I examine signatures of positive selection across the order Carnivora. The chapter aims to look for trends within and between TLRs using tests for selection, location of positively selected codons (PSCs), and TLR cellular location. I also investigate strength of selection over each species’ evolutionary history to find relationships with ecological and life history characteristics. The majority of TLRs show robust evidence of positive selection, with PSCs located within areas of biological significance for pathogen interaction. Stronger signs of positive selection were found in extra-cellular receptors than intra-cellular. Significant relationships between strength of selection and ecological characteristics and life history traits were found in multiples TLRs. Most notably, these were with the reproductive traits of gestation length, interbirth interval, and litter size, which potentially illustrate theories of life history trade off in investment between reproduction and immune function. The second chapter of this thesis focuses on genetic and behavioural defences which are crucial in host-pathogen relationships but not often combined into one study. This study looks at population-level TLR polymorphism in the bank vole (Myodes glareolus) and boldness and exploration personality scores. The haplotypes of the voles formed three clusters (A, B and C) but no significant relationships were found between the clusters and personality. However, there was a trend between B cluster haplotypes and increased explorations scores. These prospective relationships have implications in the maintenance of personality and genetic variation within populations and their roles in the spread of disease. The study highlights the importance of considering multiple aspects of host immune defence and their interactions rather than individualising the components. Overall, interaction with pathogens plays a large role in patterns in selection seen across taxa and within species. This thesis shows how the inclusion and consideration of ecological and behavioural factors into immunogenetics can provide a more representative idea of the complex interactions that are at work in host immune defences.
Abstract.
Romero-Haro AÁ, Pérez-Rodríguez L, Tschirren B (2022). Intergenerational Costs of Oxidative Stress: Reduced Fitness in Daughters of Mothers That Experienced High Levels of Oxidative Damage during Reproduction. Physiological and Biochemical Zoology, 95(1), 1-14.
Giraldo-Deck L, Loveland J, Goymann W, Tschirren B, Burke T, Kempenaers B, Lank D, Küpper C (2022). Intralocus conflicts associated with a supergene.
Nature Communications,
13Abstract:
Intralocus conflicts associated with a supergene
Chromosomal inversions frequently underlie major phenotypic variation maintained by divergent selection within and between sexes. Here we examine whether and how intralocus conflicts contribute to balancing selection stabilizing an autosomal inversion polymorphism in the ruff Calidris pugnax. In this lekking shorebird, three male mating morphs (Independents, Satellites and Faeders) are associated with an inversion-based supergene. We show that in a captive population, Faeder females, who are smaller and whose inversion haplotype has not undergone recombination, have lower average reproductive success in terms of laying rate, egg size and offspring survival than Independent females, who lack the inversion. Satellite females, who carry a recombined inversion haplotype and have intermediate body size, more closely resemble Independent than Faeder females in reproductive performance. We inferred that the lower reproductive output of Faeder females is primarily balanced by higher than average reproductive success of individual Faeder males, driven by negative frequency-dependent selection. These findings suggest that intralocus conflicts may play a major role in the evolution and maintenance of supergene variants.
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Råberg L, Clough D, Hagström Å, Scherman K, Andersson M, Drews A, Strandh M, Tschirren B, Westerdahl H (2022). MHC class II genotype-by-pathogen genotype interaction for infection prevalence in a natural rodent-Borrelia system.
Evolution,
76(9), 2067-2075.
Abstract:
MHC class II genotype-by-pathogen genotype interaction for infection prevalence in a natural rodent-Borrelia system.
MHC genes are extraordinarily polymorphic in most taxa. Host-pathogen coevolution driven by negative frequency-dependent selection (NFDS) is one of the main hypotheses for the maintenance of such immunogenetic variation. Here, we test a critical but rarely tested assumption of this hypothesis-that MHC alleles affect resistance/susceptibility to a pathogen in a strain-specific way, that is, there is a host genotype-by-pathogen genotype interaction. In a field study of bank voles naturally infected with the tick-transmitted bacterium Borrelia afzelii, we tested for MHC class II (DQB) genotype-by-B. afzelii strain interactions for infection prevalence between 10 DQB alleles and seven strains. One allele (DQB*37) showed an interaction, such that voles carrying DQB*37 had higher prevalence of two strains and lower prevalence of one strain than individuals without the allele. These findings were corroborated by analyses of strain composition of infections, which revealed an effect of DQB*37 in the form of lower β diversity among infections in voles carrying the allele. Taken together, these results provide rare support at the molecular genetic level for a key assumption of models of antagonistic coevolution through NFDS.
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Hsu B, Pakanen V, Boner W, Doligez B, Eeva T, Groothuis TGG, Korpimäki E, Laaksonen T, Lelono A, Monaghan P, et al (2022). Maternally transferred thyroid hormones and life‐history variation in birds.
Journal of Animal Ecology,
91(7), 1489-1506.
Abstract:
Maternally transferred thyroid hormones and life‐history variation in birds
AbstractIn vertebrates, thyroid hormones (THs) play an important role in the regulation of growth, development, metabolism, photoperiodic responses and migration. Maternally transferred THs are important for normal early phase embryonic development when embryos are not able to produce endogenous THs. Previous studies have shown that variation in maternal THs within the physiological range can influence offspring phenotype.Given the essential functions of maternal THs in development and metabolism, THs may be a mediator of life‐history variation across species.We tested the hypothesis that differences in life histories are associated with differences in maternal TH transfer across species. Using birds as a model, we specifically tested whether maternally transferred yolk THs covary with migratory status, developmental mode and traits related to pace‐of‐life (e.g. basal metabolic rate, maximum life span).We collected un‐incubated eggs (n = 1–21 eggs per species, median = 7) from 34 wild and captive bird species across 17 families and six orders to measure yolk THs [both triiodothyronine (T3) and thyroxine (T4)], compiled life‐history trait data from the literature and used Bayesian phylogenetic mixed models to test our hypotheses.Our models indicated that both concentrations and total amounts of the two main forms of THs (T3 and T4) were higher in the eggs of migratory species compared to resident species, and total amounts were higher in the eggs of precocial species, which have longer prenatal developmental periods, than in those of altricial species. However, maternal yolk THs did not show clear associations with pace‐of‐life‐related traits, such as fecundity, basal metabolic rate or maximum life span.We quantified interspecific variation in maternal yolk THs in birds, and our findings suggest higher maternal TH transfer is associated with the precocial mode of development and migratory status. Whether maternal THs represent a part of the mechanism underlying the evolution of precocial development and migration or a consequence of such life histories is currently unclear. We therefore encourage further studies to explore the physiological mechanisms and evolutionary processes underlying these patterns.
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Hansford KM, Wheeler BW, Tschirren B, Medlock JM (2022). Questing Ixodes ricinus ticks and Borrelia spp. in urban green space across Europe: a review.
Zoonoses Public Health,
69(3), 153-166.
Abstract:
Questing Ixodes ricinus ticks and Borrelia spp. in urban green space across Europe: a review.
For more than three decades, it has been recognized that Ixodes ricinus ticks occur in urban green space in Europe and that they harbour multiple pathogens linked to both human and animal diseases. Urban green space use for health and well-being, climate mitigation or biodiversity goals is promoted, often without consideration for the potential impact on tick encounters or tick-borne disease outcomes. This review synthesizes the results of over 100 publications on questing I. ricinus and Borrelia spp. infections in ticks in urban green space in 24 European countries. It presents data on several risk indicators for Lyme borreliosis and highlights key research gaps and recommendations for future studies. Across Europe, mean density of I. ricinus in urban green space was 6.9 (range; 0.1-28.8) per 100 m2 and mean Borrelia prevalence was 17.3% (range; 3.1%-38.1%). Similar density estimates were obtained for nymphs, which had a Borrelia prevalence of 14.2% (range; 0.5%-86.7%). Few studies provided data on both questing nymph density and Borrelia prevalence, but those that did found an average of 1.7 (range; 0-5.6) Borrelia-infected nymphs per 100 m2 of urban green space. Although a wide range of genospecies were reported, Borrelia afzelii was the most common in most parts of Europe, except for England where B. garinii was more common. The emerging pathogen Borrelia miyamotoi was also found in several countries, but with a much lower prevalence (1.5%). Our review highlights that I. ricinus and tick-borne Borrelia pathogens are found in a wide range of urban green space habitats and across several seasons. The impact of human exposure to I. ricinus and subsequent Lyme borreliosis incidence in urban green space has not been quantified. There is also a need to standardize sampling protocols to generate better baseline data for the density of ticks and Borrelia prevalence in urban areas.
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Romero-Haro AÁ, Morger J, Haussmann MF, Tschirren B (2022). Reproductive Strategies Affect Telomere Dynamics across the Life Course. The American Naturalist, 200(3), 373-382.
Vedder O, Bichet C, Tschirren B (2022). The Effect of Manipulated Prenatal Conditions on Growth, Survival, and Reproduction Throughout the Complete Life Course of a Precocial Bird. Frontiers in Ecology and Evolution, 10
Lemoine M, Cornetti L, Reeh K, Tschirren B (2022). Tick range expansion to higher elevations: does Borrelia burgdorferi sensu lato facilitate the colonisation of marginal habitats?.
BMC Ecol Evol,
22(1).
Abstract:
Tick range expansion to higher elevations: does Borrelia burgdorferi sensu lato facilitate the colonisation of marginal habitats?
BACKGROUND: Parasites can alter host and vector phenotype and thereby affect ecological processes in natural populations. Laboratory studies have suggested that Borrelia burgdorferi sensu lato, the causative agent of human Lyme borreliosis, may induce physiological and behavioural alterations in its main tick vector in Europe, Ixodes ricinus, which increase the tick's mobility and survival under challenging conditions. These phenotypic alterations may allow I. ricinus to colonise marginal habitats ('facilitation hypothesis'), thereby fuelling the ongoing range expansion of I. ricinus towards higher elevations and latitudes induced by climate change. To explore the potential for such an effect under natural conditions, we studied the prevalence of B. burgdorferi s.l. in questing I. ricinus and its variation with elevation in the Swiss Alps. RESULTS: We screened for B. burgdorferi s.l. infection in questing nymphs of I. ricinus (N = 411) from 15 sites between 528 and 1774 m.a.s.l to test if B. burgdorferi s.l. prevalence is higher at high elevations (i.e. in marginal habitats). Opposite of what is predicted under the facilitation hypothesis, we found that B. burgdorferi s.l. prevalence in I. ricinus nymphs decreased with increasing elevation and that Borrelia prevalence was 12.6% lower in I. ricinus nymphs collected at the range margin compared to nymphs in the core range. But there was no association between Borrelia prevalence and elevation within the core range of I. ricinus. Therefore the observed pattern was more consistent with a sudden decrease in Borrelia prevalence above a certain elevation, rather than a gradual decline with increasing elevation across the entire tick range. CONCLUSIONS: in conclusion, we found no evidence that B. burgdorferi s.l.-induced alterations of I. ricinus phenotype observed in laboratory studies facilitate the colonisation of marginal habitats in the wild. Rather, ticks in marginal habitats are substantially less likely to harbour the pathogen. These findings have implications for a better understanding of eco-evolutionary processes in natural host-parasite systems, as well as the assessment of Lyme borreliosis risk in regions where I. ricinus is newly emerging.
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Hansford KM, Wheeler BW, Tshirren B, Medlock JM (2022). Urban woodland habitat is important for tick presence and density in a city in England.
Ticks and Tick-borne Diseases,
13(1).
Abstract:
Urban woodland habitat is important for tick presence and density in a city in England
Urban green spaces provide an opportunity for contact between members of the public and ticks infected with pathogens. Understanding tick distribution within these areas and the drivers for increased tick density or Borrelia infection are important from a risk management perspective. This study aimed to generate data on tick presence, nymph density and Borrelia infection across a range of urban green space habitats, in order to identify those that may potentially present a higher risk of Lyme borreliosis to members of the public. Several sites were visited across the English city of Bath during 2015 and 2016. Tick presence was confirmed in all habitats surveyed, with increased likelihood in woodland and woodland edge. Highest nymph densities were also reported in these habitats, along with grassland during one of the sampling years. Adult ticks were more likely to be infected compared to nymphs, and the highest densities of infected nymphs were associated with woodland edge habitat. In addition to Lyme borreliosis causing Borrelia genospecies, Borrelia miyamotoi was also detected at several sites. This study adds to the growing evidence that urban green space habitats present a public health risk from tick bites, and this has implications for many policy areas including health and wellbeing, climate adaptation and urban green space planning.
Abstract.
2021
Aivelo T, Lemoine M, Tschirren B (2021). Elevational changes in bacterial microbiota structure and diversity in an arthropod-disease vector.
Microbial EcologyAbstract:
Elevational changes in bacterial microbiota structure and diversity in an arthropod-disease vector
Environmental conditions change rapidly along elevational gradients and have been found to affect community composition in macroscopic taxa, with lower diversity typically observed at higher elevations. In contrast, microbial community responses to elevation are still poorly understood. Specifically, the effects of elevation on vector-associated microbiota have not been studied to date, even though the within-vector microbial community is known to influence vector competence for a range of zoonotic pathogens. Here we characterize the structure and diversity of the bacterial microbiota in an important zoonotic disease vector, the sheep tick Ixodes ricinus, along replicated elevational gradient (630–1673 m) in the Swiss Alps. 16S rRNA sequencing of the whole within-tick bacterial microbiota of questing nymphs and adults revealed a decrease in Faith’s phylogenetic microbial alpha diversity with increasing elevation, while beta diversity analyses revealed a lower variation in microbial community composition at higher elevations. We also found a higher microbial diversity later in the season and significant differences in microbial diversity among tick life stages and sexes, with lowest microbial alpha diversity observed in adult females. No associations between tick genetic diversity and bacterial diversity were observed. Our study demonstrates systematic changes in tick bacterial microbiota diversity along elevational gradients. The observed patterns mirror diversity changes along elevational gradients typically observed in macroscopic taxa, and they highlight the key role of environmental factors in shaping within-host microbial communities in ectotherms.
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Full text.
Aivelo T, Lemoine M, Tschirren B (2021). Elevational changes in bacterial microbiota structure and diversity in an arthropod-disease vector.
Abstract:
Elevational changes in bacterial microbiota structure and diversity in an arthropod-disease vector
Environmental conditions change rapidly along elevational gradients and have been found to affect community composition in macroscopic taxa, with lower diversity typically observed at higher elevations. In contrast, microbial community responses to elevation are still poorly understood. Specifically, the effects of elevation on vector-associated microbiota have not been studied to date, even though the within-vector microbial community is known to influence vector competence for a range of zoonotic pathogens. Here we characterize the structure and diversity of the bacterial microbiota in an important zoonotic disease vector, the sheep tick Ixodes ricinus , along replicated elevational gradient (630 - 1673 masl) in the Swiss Alps. 16S rRNA sequencing of the whole within-tick bacterial microbiota of questing nymphs and adults revealed a decrease in Faith’s phylogenetic microbial alpha diversity with increasing elevation, while beta diversity analyses revealed a lower variation in microbial community composition at higher elevations. We also found a higher microbial diversity later in the season and significant differences in microbial diversity among tick life stages and sexes, with lowest microbial alpha diversity observed in adult females. No associations between tick genetic diversity and bacterial diversity were observed. Our study demonstrates systematic changes in tick bacterial microbiota diversity along elevational gradients. The observed patterns mirror diversity changes along elevational gradients typically observed in macroscopic taxa, and they highlight the key role of environmental factors in shaping within-host microbial communities in ectotherms.
Abstract.
Tschirren B, Romero-Haro AÁ, Zahn S, Criscuolo F (2021). Sex-specific effects of experimental ectoparasite infestation on telomere length in great tit nestlings.
J Evol Biol,
34(3), 584-589.
Abstract:
Sex-specific effects of experimental ectoparasite infestation on telomere length in great tit nestlings.
Telomere length is a biomarker of biological ageing and lifespan in various vertebrate taxa. Evidence is accumulating that telomeres shorten more rapidly when an individual is exposed to environmental stressors. Parasites are potent selective agents that can cause physiological stress directly or indirectly through the activation of the host's immune system. Yet to date, empirical evidence for a role of parasites in telomere dynamics in natural populations is limited. Here, we show experimentally that exposure to ectoparasitic hen fleas (Ceratophyllus gallinae) during growth results in shorter telomeres in female, but not male, great tit (Parus major) nestlings. Females had longer telomeres than males when growing up in experimentally deparasitized nests but, likely because of the sex-specific effects of ectoparasitism on telomere length, this sexual dimorphism was absent in birds growing up in experimentally infested nests. Our results provide the first experimental evidence for a role of ectoparasitism in telomere dynamics in a natural vertebrate population, and suggest that the costs of infection manifest in sex-specific ways.
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Author URL.
Bladen C (2021). The relationships between testes asymmetry, seminiferous composition and the quality and quantity of sperm produced in a precocial bird.
Abstract:
The relationships between testes asymmetry, seminiferous composition and the quality and quantity of sperm produced in a precocial bird
Theory assumes that postcopulatory sexual selection favours increased investment into testes size, as larger testes produce ejaculates that provide a competitive advantage when rival males compete for fertilisation. However, the relationship between relative increases in testes size with the organisation of sperm-producing tissue, and how such changes influence sperm quality and quantity is not fully understood. Male Japanese quail (Coturnix japonica) originating from lines artificially selected for high female reproductive investment experienced higher fertilisation success, as well as a relatively larger left testis than males from low reproductive investment lines. The aim of this study was to determine the origin of this increased fertility from a morphological perspective. For males from both lines and in both testis, we measured the proportion and absolute amount of seminiferous tissue, as well as the quantity and quality of sperm within the sperm reserves, including sperm length and proportions that were alive and morphologically normal. The left testis of high line males had higher proportions of interstitial tissue, but not seminiferous tissue, and did not produce different sperm morphologies that could explain the enhanced fertilisation success. On the contrary, the right testis had higher proportions of seminiferous tissue and produced more alive sperm. There was no difference in sperm quantity or proportions of sperm with normal morphology in either testis of males from divergent lines. Independently of line origin, the right testis contained sperm with larger tails, total lengths, and shorter ratios of the head : tail, indicating a specialisation to produce faster sperm. Overall, we found no clear difference in the quality or quantity of sperm produced by high line males that could explain their reproductive success. However, because ejaculates are complex, interactive, multivariate traits, fertilisation success could have been influenced by other traits not measured here, such as the composition of copulatory fluids, functions of somatic cells in the testes, provisioning against oxidative stress or the regulation of sperm use by the females. Altogether, these results highlight unusual relationships between testes size with testes and sperm morphology and demonstrate that relatively larger testes do not necessarily have more seminiferous tissue or produce more, or better quality sperm.
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2020
Pick JL, Hatakeyama M, Ihle KE, Gasparini J, Haussy C, Ishishita S, Matsuda Y, Yoshimura T, Kanaoka MM, Shimizu-Inatsugi R, et al (2020). Artificial selection reveals the role of transcriptional constraints in the maintenance of life history variation. Evolution Letters
Aivelo T, Tschirren B (2020). Bacterial microbiota composition of a common ectoparasite of cavity-breeding birds, the Hen Flea Ceratophyllus gallinae. IBIS: the International Journal of Avian Science
Cornetti L, Tschirren B (2020). Combining genome-wide association study and FST-based approaches to identify targets of Borrelia-mediated selection in natural rodent hosts.
Molecular Ecology,
29 (7), 1386-1397.
Abstract:
Combining genome-wide association study and FST-based approaches to identify targets of Borrelia-mediated selection in natural rodent hosts
Recent advances in high-throughput sequencing technologies provide opportunities to gain novel insights into the genetic basis of phenotypic trait variation. Yet to date, progress in our understanding of genotype-phenotype associations in non-model organisms in general and natural vertebrate populations in particular has been hampered by small sample sizes typically available for wildlife populations and a resulting lack of statistical power, as well as a limited ability to control for false positive signals. Here we propose to combine a genome-wide association (GWAS) and FST-based approach with population-level replication to partly overcome these limitations. We present a case study in which we used this approach in combination with Genotyping-by-Sequencing (GBS) SNP data to identify genomic regions associated with Borrelia afzelii resistance or susceptibility in the natural rodent host of this Lyme disease-causing spirochete, the bank vole (Myodes glareolus). Using this combined approach we identified four consensus SNPs located in exonic regions of the genes Slc26a4, Tns3, Wscd1 and Espnl, which were significantly associated with the voles’ Borrelia infectious status within and across populations. Functional links between host responses to bacterial infections and most of these genes have previously been demonstrated in other rodent systems, making them promising new candidates for the study of evolutionary host responses to Borrelia emergence. Our approach is applicable to other systems and may facilitate the identification of genetic variants underlying disease resistance or susceptibility, as well as other ecologically relevant traits, in wildlife populations.
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EL-Andari R, Cunha F, Tschirren B, Iwaniuk AN (2020). Selection for divergent reproductive investment affects neuron size and foliation in the cerebellum. Brain, Behavior and Evolution, 95, 69-77.
Loukola OJ, Adamik P, Adriaensen F, Barba E, Doligez B, Flensted‐Jensen E, Eeva T, Kivelä SM, Laaksonen T, Morosinotto C, et al (2020). The roles of temperature, nest predators and information parasites for geographical variation in egg covering behaviour of tits (Paridae). Journal of Biogeography
2019
Aivelo T, Norberg A, Tschirren B (2019). Bacterial microbiota composition of Ixodes ricinus ticks: the role of environmental variation, tick characteristics and microbial interactions. PeerJ, 7, e8217-e8217.
Groothuis TGG, Hsu B-Y, Kumar N, Tschirren B (2019). Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model. Philosophical Transactions B: Biological Sciences
Pick JL, Postma E, Tschirren B (2019). The more you get, the more you give: Positive cascading effects shape the evolutionary potential of prenatal maternal investment.
Evol Lett,
3(4), 412-423.
Abstract:
The more you get, the more you give: Positive cascading effects shape the evolutionary potential of prenatal maternal investment.
Maternal effects are prevalent in nature and significantly contribute to variation in phenotypic trait expression. However, little attention has been paid to the factors shaping variation in the traits mediating these effects (maternal effectors). Specific maternal effectors are often not identified, and typically they are assumed to be inherited in an additive genetic and autosomal manner. Given that these effectors can cause long-lasting effects on offspring phenotype, it is likely that they may also affect themselves in the next generation. Although the existence of such cascading maternal effects has been discussed and modeled, empirical examples of such effects are rare, let alone quantitative estimates of their strength and evolutionary consequences. Here, we demonstrate that the investment a mother makes in her eggs positively affects the egg investment of her daughters. Through reciprocally crossing artificially selected lines for divergent prenatal maternal investment in Japanese quail (Coturnix japonica), we demonstrate that the size of eggs daughters lay resembles the egg size of their maternal line significantly more than that of their paternal line, highlighting that egg size is in part maternally inherited. Correspondingly, we find that variation in the daughters' egg size is in part determined by maternal identity, in addition to substantial additive genetic effects. Furthermore, this maternal variance in offspring egg size is fully explained by maternal egg size, demonstrating the presence of a positive cascading effect of maternal egg size on offspring egg size. Finally, we use an evolutionary model to quantify the consequences of covariance between cascading maternal and additive genetic effects for both maternal effector and offspring body mass evolution. Our study demonstrates that by amplifying the amount of variation available for selection to act on, positive cascading maternal effects can significantly enhance the evolutionary potential of maternal effectors and the offspring traits that they affect.
Abstract.
Author URL.
2018
Giraudeau M, Ziegler A-K, McGraw K, Okuliarova M, Zeman M, Tschirren B (2018). In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs.
Biology Letters,
14(6).
Abstract:
In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs
Mothers can influence prenatal conditions by varying the amount of nutrients, hormones or antioxidants they provide to their developing young. Some of these substances even affect the transfer of these compounds in the next generation, but it is less clear how different maternally transmitted compounds interact with each other to shape reproductive resource allocation in their offspring. Here, we found that female Japanese quail that were exposed to high carotenoid levels during embryonic development transferred lower concentrations of yolk antioxidants to their own eggs later in life. This effect disappeared, when both testosterone and carotenoid concentrations were manipulated simultaneously, showing long-term and interactive effects of these maternally derived egg components on a female’s own egg composition. Given that exposure to high levels of testosterone during embryo development stimulates the production of reactive oxygen (ROS) and impairs antioxidant defenses, we propose that carotenoids act as in-ovo antioxidants in an oxidatively stressful environment (i.e. when levels of testosterone are high) but might have prooxidant properties in an environment where they are not used to counteract an increased production of ROS. In line with this hypothesis, we previously showed that prenatal exposure to increased concentrations of yolk carotenoids leads to a rise of oxidative damage at adulthood, but only when yolk testosterone concentrations were not experimentally increased as well. As a consequence, antioxidants in the body may be used to limit oxidative damage in females exposed to high levels of carotenoids during development (but not in females exposed to increased levels of both carotenoids and testosterone), resulting in lower amounts of antioxidants being available for deposition into eggs. Since prenatal antioxidant exposure is known to influence fitness-related traits, the effect detected in this study might have transgenerational consequences.
Abstract.
Stier A, Tschirren B, Metclafe N, Monaghan P (2018). Prenatal environment as a modulator of mitochondrial function: new insights from an avian model. Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB). 3rd - 7th Jan 2018.
Cornetti L, Hilfiker D, Lemoine M, Tschirren B (2018). Small-scale spatial variation in infection risk shapes the evolution of a Borrelia resistance gene in wild rodents.
Molecular EcologyAbstract:
Small-scale spatial variation in infection risk shapes the evolution of a Borrelia resistance gene in wild rodents
Spatial variation in pathogen-mediated selection is predicted to influence the evolutionary trajectory of host populations and lead to spatial variation in their immunogenetic composition. However, to date few studies have been able to directly link small-scale spatial variation in infection risk to host immune gene evolution in natural, non-human populations. Here we use a natural rodent-Borrelia system to test for associations between landscape-level spatial variation in Borrelia infection risk along replicated elevational gradients in the Swiss Alps and Toll-like receptor 2 (TLR2) evolution, a candidate gene for Borrelia resistance, across bank vole (Myodes glareolus) populations. We found that Borrelia infection risk (i.e. the product of Borrelia prevalence in questing ticks and the average tick load of voles at a sampling site) was spatially variable and significantly negatively associated with elevation. Across sampling sites, Borrelia prevalence in bank voles was significantly positively associated with Borrelia infection risk along the elevational clines. We observed a significant association between naturally occurring TLR2 polymorphisms in hosts and their Borrelia infection status. The TLR2 variant associated with a reduced likelihood of Borrelia infection was most common in rodent populations at lower elevations that face a high Borrelia infection risk, and its frequency changed in accordance with the change in Borrelia infection risk along the elevational clines. These results suggest that small-scale spatial variation in parasite-mediated selection affects the immunogenetic composition of natural host populations, providing a striking example that the microbial environment shapes the evolution of the host’s immune system in the wild.
Abstract.
2017
Pick JL, Hutter P, Tschirren B (2017). Divergent artificial selection for female reproductive investment has a sexually concordant effect on male reproductive success.
Evolution Letters,
1(4), 222-228.
Abstract:
Divergent artificial selection for female reproductive investment has a sexually concordant effect on male reproductive success
AbstractDepending on the genetic architecture of male and female fitness, sex-specific selection can have negative, positive, or neutral consequences for the opposite sex. Theory predicts that conflict between male and female function may drive the breakdown of intrasexual genetic correlations, allowing sexual dimorphism in sexually antagonistic traits. Reproductive traits are the epitome of this, showing highly differentiated proximate functions between the sexes. Here we use divergent artificial selection lines for female reproductive investment to test how female-specific selection on a sex-limited trait affects male reproductive success in a precocial bird, the Japanese quail (Coturnix japonica). We demonstrate that selection for increased egg investment in females positively affects male reproductive success both in competitive and non-competitive mating situations. This increased reproductive success was linked to a relatively larger left testis in males originating from lines selected for high female reproductive investment. Given that female quail have functional gonads only on their left side, this correlated response indicates that selection has acted on the shared developmental basis of male and female gonads. Our study thereby provides evidence for a positive genetic correlation between key reproductive traits in males and females despite a high degree of sexual dimorphism, and suggests that, in this system, selection on reproductive function is sexually concordant.
Abstract.
Råberg L, Hagström, Andersson M, Bartkova S, Scherman K, Strandh M, Tschirren B (2017). Evolution of antigenic diversity in the tick-transmitted bacterium Borrelia afzelii: a role for host specialization?.
Journal of Evolutionary Biology,
30(5), 1034-1041.
Abstract:
Evolution of antigenic diversity in the tick-transmitted bacterium Borrelia afzelii: a role for host specialization?
Antigenic diversity in pathogenic microbes can be a result of at least three different processes: diversifying selection by acquired immunity, host–pathogen coevolution and/or host specialization. Here, we investigate whether host specialization drives diversity at ospC (which encodes an immunodominant surface protein) in the tick-transmitted bacterium Borrelia afzelii. We determined prevalence and infection intensity of ospC strains in naturally infected wild mammals (rodents and shrews) by 454 amplicon sequencing in combination with qPCR. Neither prevalence nor infection intensity of specific ospC strains varied in a species-specific manner (i.e. there were no significant ospC × host species interactions). Rankings of ospC prevalences were strongly positively correlated across host species. Rankings of ospC infection intensities were correlated more weakly, but only in one case significantly
Abstract.
Ihle KE, Hutter P, Tschirren B (2017). Increased prenatal maternal investment reduces inbreeding depression in offspring.
Proc Biol Sci,
284(1860).
Abstract:
Increased prenatal maternal investment reduces inbreeding depression in offspring.
Inbreeding depression refers to the reduction of fitness that results from matings between relatives. Evidence for reduced fitness in inbred individuals is widespread, but the strength of inbreeding depression varies widely both within and among taxa. Environmental conditions can mediate this variation in the strength of inbreeding depression, with environmental stress exacerbating the negative consequences of inbreeding. Parents can modify the environment experienced by offspring, and have thus the potential to mitigate the negative consequences of inbreeding. While such parental effects have recently been demonstrated during the postnatal period, the role of prenatal parental effects in influencing the expression of inbreeding depression remains unexplored. To address this gap, we performed matings between full-sibs or unrelated individuals in replicated lines of Japanese quail (Coturnix japonica) experimentally selected for high and low maternal egg provisioning. We show that in the low maternal investment lines hatching success was strongly reduced when parents were related. In the high maternal investment lines, however, this negative effect of inbreeding on hatching success was absent, demonstrating that prenatal maternal provisioning can alleviate the negative fitness consequences of inbreeding.
Abstract.
Author URL.
Giraudeau M, Ziegler AK, Ducatez S, Mcgraw KJ, Tschirren B, Giraudeau M (2017). Interactive and Long-term Effects of Yolk Androgens and Antioxidants in Birds.
Author URL.
Giraudeau M, Ziegler A-K, Pick JL, Ducatez S, Canale CI, Tschirren B (2017). Interactive effects of yolk testosterone and carotenoid on prenatal growth and offspring physiology in a precocial bird.
BEHAVIORAL ECOLOGY,
28(1), 31-38.
Author URL.
2016
Ebneter C, Pick JL, Tschirren B (2016). A trade-off between reproductive investment and maternal cerebellum size in a precocial bird.
Biology Letters,
12(12).
Abstract:
A trade-off between reproductive investment and maternal cerebellum size in a precocial bird
Natural selection favours increased investment in reproduction, yet considerable variation in parental investment is observed in natural populations. Life-history theory predicts that this variation is maintained by a trade-off between the benefits of increased reproductive investment and its associated costs for the parents. The nature of these costs of reproduction, however, remains poorly understood. The brain is an energetically highly expensive organ and increased reproductive investment may, therefore, negatively affect brain maintenance. Using artificial selection lines for high and low prenatal maternal investment in a precocial bird, the Japanese quail (Coturnix japonica), we provide experimental evidence for this hypothesis by showing that increased prenatal provisioning negatively affects the size of a particular brain region of the mother, the cerebellum. Our finding suggests that cognitive demands may constrain the evolution of parental investment, and vice versa, contributing to the maintenance of variation in reproductive behaviour in animal populations.
Abstract.
Pick JL, Hutter P, Ebneter C, Ziegler AK, Giordano M, Tschirren B (2016). Artificial selection reveals the energetic expense of producing larger eggs.
Frontiers in Zoology,
13(1).
Abstract:
Artificial selection reveals the energetic expense of producing larger eggs
Background: the amount of resources provided by the mother before birth has important and long-lasting effects on offspring fitness. Despite this, there is a large amount of variation in maternal investment seen in natural populations. Life-history theory predicts that this variation is maintained through a trade-off between the benefits of high maternal investment for the offspring and the costs of high investment for the mother. However, the proximate mechanisms underlying these costs of reproduction are not well understood. Here we used artificial selection for high and low maternal egg investment in a precocial bird, the Japanese quail (Coturnix japonica) to quantify costs of maternal reproductive investment. Results: We show that females from the high maternal investment lines had significantly larger reproductive organs, which explained their overall larger body mass, and resulted in a higher resting metabolic rate (RMR). Contrary to our expectations, this increase in metabolic activity did not lead to a higher level of oxidative damage. Conclusions: This study is the first to provide experimental evidence for metabolic costs of increased per offspring investment.
Abstract.
Pick JL, Ebneter C, Hutter P, Tschirren B (2016). Disentangling genetic and prenatal maternal effects on offspring size and survival.
American Naturalist,
188(6), 628-639.
Abstract:
Disentangling genetic and prenatal maternal effects on offspring size and survival
Organizational processes during prenatal development can have long-term effects on an individual’s phenotype. Because these early developmental stages are sensitive to environmental influences,mothers are in a unique position to alter their offspring’s phenotype by differentially allocating resources to their developing young. However,such prenatal maternal effects are difficult to disentangle from other forms of parental care,additive genetic effects,and/or other forms of maternal inheritance,hampering our understanding of their evolutionary consequences. Here we used divergent selection lines for high and low prenatal maternal investment and their reciprocal line crosses in a precocial bird—the Japanese quail (Coturnix japonica)—to quantify the relative importance of genes and prenatal maternal effects in shaping offspring phenotype. Maternal but not paternal origin strongly affected offspring body size and survival throughout development. Although the effects of maternal egg investment faded over time,they were large at key life stages. Additionally,there was evidence for other forms of maternal inheritance affecting offspring phenotype at later stages of development. Our study is among the first to successfully disentangle prenatal maternal effects from all other sources of confounding variation and highlights the important role of prenatal maternal provisioning in shaping offspring traits closely linked to fitness.
Abstract.
Laine VN, Gossmann TI, Schachtschneider KM, Garroway CJ, Madsen O, Verhoeven KJF, De Jager V, Megens HJ, Warren WC, Minx P, et al (2016). Evolutionary signals of selection on cognition from the great tit genome and methylome.
Nature Communications,
7Abstract:
Evolutionary signals of selection on cognition from the great tit genome and methylome
For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.
Abstract.
Tschirren B, Ziegler A-K, Canale CI, Okuliarová M, Zeman M, Giraudeau M (2016). High Yolk Testosterone Transfer is Associated with an Increased Female Metabolic Rate.
Physiol Biochem Zool,
89(5), 448-452.
Abstract:
High Yolk Testosterone Transfer is Associated with an Increased Female Metabolic Rate.
Yolk androgens of maternal origin are important mediators of prenatal maternal effects. Although in many species short-term benefits of exposure to high yolk androgen concentrations for the offspring have been observed, females differ substantially in the amount of androgens they transfer to their eggs. It suggests that costs for the offspring or the mother constrain the evolution of maternal hormone transfer. However, to date, the nature of these costs remains poorly understood. Unlike most previous work that focused on potential costs for the offspring, we here investigated whether high yolk testosterone transfer is associated with metabolic costs (i.e. a higher metabolic rate) for the mother. We show that Japanese quail (Coturnix japonica) females that deposit higher testosterone concentrations into their eggs have a higher resting metabolic rate. Because a higher metabolic rate is often associated with a shorter life span, this relationship may explain the negative association between yolk testosterone transfer and female longevity observed in the wild. Our results suggest that metabolic costs for the mother can balance the short-term benefits of yolk testosterone exposure for the offspring, thereby contributing to the maintenance of variation in maternal yolk hormone transfer in natural populations.
Abstract.
Author URL.
Cornetti L, Lemoine M, Hilfiker D, Morger J, Reeh K, Tschirren B (2016). Higher genetic diversity on mountain tops: the role of historical and contemporary processes in shaping genetic variation in the bank vole.
Biological Journal of the Linnean Society,
118(2), 233-244.
Abstract:
Higher genetic diversity on mountain tops: the role of historical and contemporary processes in shaping genetic variation in the bank vole
Glacial phases during the Pleistocene caused remarkable changes in species range distributions, with inevitable genetic consequences. Specifically, during interglacial phases, when the ice melted and new habitats became suitable again, species could recolonize regions that were previously covered by ice, such as high latitudes and elevations. Based on theoretical models and empirical data, a decrease in genetic variation is predicted along recolonization routes as a result of the consecutive founder effects that characterize the recolonization process. In the present study, we assessed the relative importance of historical and contemporary processes in shaping genetic diversity and differentiation of bank vole (Myodes glareolus) populations at different elevations in the Swiss Alps. By contrast to expectations, we found that genetic variation increased with elevation. Estimates of recent migration rates and a contrasting pattern of genetic differentiation observed at the mitochondrial cytochrome b gene and nuclear microsatellites support the hypothesis that higher genetic diversity at high elevation results from contemporary gene flow. Although historical recolonization processes can have marked effects on the genetic structure of populations, the present study provides an example where contemporary processes along an environmental gradient can reverse predicted patterns of genetic variation.
Abstract.
Pick JL, Hutter P, Tschirren B (2016). In search of genetic constraints limiting the evolution of egg size: Direct and correlated responses to artificial selection on a prenatal maternal effector.
Heredity,
116(6), 542-549.
Abstract:
In search of genetic constraints limiting the evolution of egg size: Direct and correlated responses to artificial selection on a prenatal maternal effector
Maternal effects are an important force in nature, but the evolutionary dynamics of the traits that cause them are not well understood. Egg size is known to be a key mediator of prenatal maternal effects with an established genetic basis. In contrast to theoretical expectations for fitness-related traits, there is a large amount of additive genetic variation in egg size observed in natural populations. One possible mechanism for the maintenance of this variation is through genetic constraints caused by a shared genetic basis among traits. Here we created replicated, divergent selection lines for maternal egg investment in Japanese quail (Coturnix japonica) to quantify the role of genetic constraints in the evolution of egg size. We found that egg size responds rapidly to selection, accompanied by a strong response in all egg components. Initially, we observed a correlated response in body size, but this response declined over time, showing that egg size and body size can evolve independently. Furthermore, no correlated response in fecundity (measured as the proportion of days on which a female laid an egg) was observed. However, the response to selection was asymmetrical, with egg size plateauing after one generation of selection in the high but not the low investment lines. We attribute this pattern to the presence of genetic asymmetries, caused by directional dominance or unequal allele frequencies. Such asymmetries may contribute to the evolutionary stasis in egg size observed in natural populations, despite a positive association between egg size and fitness.
Abstract.
Giraudeau M, Ziegler A-K, Tschirren B (2016). Long-term effect of yolk carotenoid levels on testis size in a precocial bird.
Biol Lett,
12(4).
Abstract:
Long-term effect of yolk carotenoid levels on testis size in a precocial bird.
Conditions experienced during prenatal development can have long-lasting organizational effects on offspring. Maternal carotenoids deposited in the eggs of birds and other oviparous species play an important role during fast embryonic growth and chick development through their antioxidant properties. However, the long-term consequences of variation in maternal carotenoid transfer for the offspring have seldom been considered. Since plasma carotenoid levels at adulthood are known to influence testis size and yolk carotenoid levels influence the ability to extract carotenoids later in life, we hypothesized that maternally transmitted carotenoids might influence gonad size at adulthood. Here, we showed that male Japanese quail (Coturnix japonica) originating from a carotenoid-enriched egg had smaller testes than control individuals at adulthood. This result shows that yolk carotenoids have long-term organizational effects. In addition, given that carotenoid intake at sexual maturity increases sperm quality and that a decreased testis size is associated with a lower sperm production, we propose that carotenoid exposure during embryo development might influence a trade-off between ejaculate size and sperm quality.
Abstract.
Author URL.
Tschirren B, Ziegler AK, Pick JL, Okuliarová M, Zeman M, Giraudeau M (2016). Matrilineal inheritance of a key mediator of prenatal maternal effects.
Proceedings of the Royal Society B: Biological Sciences,
283(1838).
Abstract:
Matrilineal inheritance of a key mediator of prenatal maternal effects
© 2016 the Author(s) Published by the Royal Society. Sex-linkage is predicted to evolve in response to sex-specific or sexually antagonistic selection. In line with this prediction, most sex-linked genes are associated with reproduction in the respective sex. In addition to traits directly involved in fertility and fecundity, mediators of maternal effects may be predisposed to evolve sex-linkage, because they indirectly affect female fitness through their effect on offspring phenotype. Here, we test for sex-linked inheritance of a key mediator of prenatal maternal effects in oviparous species, the transfer of maternally derived testosterone to the eggs. Consistent with maternal inheritance, we found that in Japanese quail (Coturnix japonica) granddaughters resemble their maternal (but not their paternal) grandmother in yolk testosterone deposition. This pattern of resemblance was not due to non-genetic priming effects of testosterone exposure during prenatal development, as an experimental manipulation of yolk testosterone levels did not affect the females’ testosterone transfer to their own eggs later in life. Instead,Wchromosome and/or mitochondrial variation may underlie the observed matrilineal inheritance pattern. Ultimately, the inheritance of mediators of maternal effects along the maternal line will allow for a fast and direct response to female-specific selection, thereby affecting the dynamics of evolutionary processes mediated by maternal effects.
Abstract.
2015
Tschirren B (2015). Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe.
Biology Letters,
11(5).
Abstract:
Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe
Although parasite-mediated selection is assumed to be the main driver of immune gene evolution, empirical evidence that parasites induce allele frequencychanges at host immune genes in time and/or space remains scarce. Here, I show that the frequency of a protective gene variant of the innate immune receptor Toll-like receptor 2 in natural bank vole (Myodes glareolus) populations is positively associated with the strength of Borrelia burgdorferi sensu lato infection risk across the European continent. Thereby, this study provides rare evidence for the role of spatially variable infection pressures in moulding the vertebrate immune system.
Abstract.
Tschirren B (2015). Differential effects of maternal yolk androgens on male and female offspring: a role for sex-specific selection?.
PLoS ONE,
10(7).
Abstract:
Differential effects of maternal yolk androgens on male and female offspring: a role for sex-specific selection?
Maternal hormones are important mediators of prenatal maternal effects in animals. Although their effects on offspring phenotype are often sex-specific, the reason why sometimes sons are more sensitive to prenatal hormone exposure and sometimes daughters is not well understood. Here I combine an experimental manipulation of yolk testosterone concentration in the egg and quantification of selection acting on yolk androgen-sensitive traits in a natural population of great tits (Parus major) with a literature review to test the hypothesis that sex-specific selection on traits affected by yolk androgens determines which sex is more sensitive to prenatal hormone exposure. An experimental increase of the testosterone content in the egg boosted the post-hatching growth of male, but not female great tit nestlings. However, I found no evidence that survival selection on body mass or size is acting differently in the two sexes. A literature review revealed that yolk androgen manipulations affect the growth of males and females differently across species. Interestingly, in studies performed in the wild a significant association between the strength and direction of sexual size dimorphism and sex-specific sensitivities to yolk androgens was observed. In studies performed in captivity, no such relationship was found. Thus, across species there is some evidence that sex-specific selection on body size influences how strongly growth trajectories of males and females are affected by maternally-derived yolk androgens.
Abstract.
Morger J, Råberg L, Hille SM, Helsen S, Štefka J, Al-Sabi MM, Kapel CMO, Mappes T, Essbauer S, Ulrich RG, et al (2015). Distinct haplotype structure at the innate immune receptor Toll-like receptor 2 across bank vole populations and lineages in Europe.
Biological Journal of the Linnean Society,
116(1), 124-133.
Abstract:
Distinct haplotype structure at the innate immune receptor Toll-like receptor 2 across bank vole populations and lineages in Europe
Parasite-mediated selection may contribute to the maintenance of genetic variation at host immune genes over long time scales. To date, the best evidence for the long-term maintenance of immunogenetic variation in natural populations comes from studies on the major histocompatibility complex (MHC) genes, whereas evidence for such processes from other immune genes remains scarce. In the present study, we show that, despite pronounced population differentiation and the occurrence of numerous private alleles within populations, the innate immune gene Toll-like receptor 2 (TLR2) displays a distinct haplotype structure in 21 bank vole (Myodes glareolus) populations across Europe. Haplotypes from all populations grouped in four clearly differentiated clusters, with the three main clusters co-occurring in at least three previously described mitochondrial lineages. This pattern indicates that the distinct TLR2 haplotype structure may precede the split of the mitochondrial lineages 0.19-0.56 Mya and suggests that haplotype clusters at this innate immune receptor are maintained over prolonged time in wild bank vole populations.
Abstract.
Giordano M, Costantini D, Pick JL, Tschirren B (2015). Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits.
Behavioral Ecology and Sociobiology,
69(5), 777-785.
Abstract:
Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits
Oxidative stress has been suggested as a mechanism underlying the costs of reproduction and life history trade-offs. Reproductive activities may lead to high production of pro-oxidants, whose activity can generate oxidative damage when not countered by adequate antioxidant defenses. Because inter-individual differences in the efficiency of the antioxidant system are influenced by an individual’s diet, food availability experienced during reproduction may affect the females’ antioxidant status and, in birds, their ability to transfer antioxidants into their eggs. Moreover, a female’s ability to cope with oxidative stress has been suggested to influence pigment deposition in the eggshell, suggesting a possible signaling function of eggshell maculation. Here we performed a food supplementation experiment in a natural population of great tits (Parus major) in order to investigate how nutritional conditions experienced during the egg laying period affect the female’s oxidative status and egg investment and how maternal oxidative status and egg antioxidant protection relate to eggshell pigmentation. We show that food-supplemented females had lower oxidative damage levels (ROMs) than non-food-supplemented females. Furthermore, a female’s ROMs levels were negatively associated with the levels of yolk antioxidant protection in her eggs, but this negative association was only significant in non-food-supplemented females. This suggests that oxidative stress experienced during reproduction influences the allocation of antioxidants into the eggs. Moreover, we observed a positive relationship between eggshell pigment distribution and maternal and yolk antioxidant protection, suggesting that eggshell pigmentation is a cue of female (and offspring) quality.
Abstract.
Giordano M, Costantini D, Tschirren B (2015). Sex-specific effects of prenatal and postnatal nutritional conditions on the oxidative status of great tit nestlings.
Oecologia,
177(1), 123-131.
Abstract:
Sex-specific effects of prenatal and postnatal nutritional conditions on the oxidative status of great tit nestlings
The early life period is characterized by fast growth and development, which can lead to high reactive oxygen species (ROS) production. Young animals thus have to balance their investment in growth versus ROS defence, and this balance is likely mediated by resource availability. Consequently resources transferred prenatally by the mother and nutritional conditions experienced shortly after birth may crucially determine the oxidative status of young animals. Here, we experimentally investigated the relative importance of pre- and early postnatal nutritional conditions on the oxidative status of great tit nestlings (Parus major). We show that resources transferred by the mother through the egg and nutritional conditions encountered after hatching affect the oxidative status of nestling in a sex-specific way. Daughters of non-supplemented mothers and daughters which did not receive extra food during the early postnatal period had higher oxidative damage than sons, while no differences between sons and daughters were found when extra food was provided pre- or postnatally. No effect of the food supplementations on growth, fledging mass or tarsus length was observed, indicating that female nestlings maintained their investment in growth at the expense of ROS defence mechanisms when resources were limited. The lower priority of the antioxidant defence system for female nestlings was also evidenced by lower levels of specific antioxidant components. These results highlight the important role of early parental effects in shaping oxidative stress in the offspring, and show that the sensitivity to these parental effects is sex-specific.
Abstract.
2014
Giordano M, Groothuis TGG, Tschirren B (2014). Interactions between prenatal maternal effects and posthatching conditions in a wild bird population.
Behavioral Ecology,
25(6), 1459-1466.
Abstract:
Interactions between prenatal maternal effects and posthatching conditions in a wild bird population
Resources and cues provided by the mother before birth are important mediators of developmental plasticity. It has been suggested that the adaptive value of such prenatal maternal effects may depend on the environment encountered by the offspring after birth, and that offspring may perform better when environmental conditions encountered by the mother and the offspring match, than when a mismatch occurs. Here, we test how prenatal maternal effects and postnatal conditions interact in influencing offspring growth and development in wild-living great tits (Parus major) by manipulating food availability experienced by the mother before egg laying, partially cross-fostering nestlings between nests, and manipulating food availability after hatching. We observed significant interaction effects between pre- and postnatal food conditions. Nonsupplemented nestlings reached a similar fledging mass, a trait closely linked to postfledging survival, as food-supplemented nestlings when their biological mother had received extra food during egg laying. It shows that prenatal maternal investment can compensate for growth-limiting conditions after hatching. This effect was sex specific, with daughters benefiting more than sons. Furthermore, food-supplemented nestlings grew largest when their biological mother had not received extra food during egg laying, suggesting that offspring were primed prenatally, possibly through differential egg composition, to use resources more efficiently. However, we found no evidence that offspring performed generally better when pre- and postnatal food conditions matched than when a mismatch occurred. Our results demonstrate the importance of considering the postnatal environment when testing for the ecological and evolutionary consequences of prenatal maternal effects in natural populations.
Abstract.
Tschirren B, Postma E, Gustafsson L, Groothuis TGG, Doligez B (2014). Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population.
Ecology Letters,
17(10), 1310-1315.
Abstract:
Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population
Maternal hormones are important mediators of prenatal maternal effects. Although many experimental studies have demonstrated their potency in shaping offspring phenotypes, we know remarkably little about their adaptive value. Using long-term data on a wild collared flycatcher (Ficedula albicollis) population, we show that natural selection acts in opposite ways on two maternally derived androgens, yolk androstenedione (A4) and yolk testosterone (T). High yolk A4 concentrations are associated with higher fitness, whereas high yolk T concentrations are associated with lower fitness. Natural selection thus favours females that produce eggs with high A4 and low T concentrations. Importantly, however, there exists a positive (non-genetic) correlation between A4 and T, which suggests that females are limited in their ability to reach this adaptive optimum. Thereby, these results provide strong evidence for an adaptive value of differential maternal androgen deposition, and a mechanistic explanation for the maintenance of variation in maternal investment in the wild.
Abstract.
Morger J, Bajnok J, Boyce K, Craig PS, Rogan MT, Lun ZR, Hide G, Tschirren B (2014). Naturally occurring Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12) polymorphisms are not associated with Toxoplasma gondii infection in wild wood mice.
Infection, Genetics and Evolution,
26, 180-184.
Abstract:
Naturally occurring Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12) polymorphisms are not associated with Toxoplasma gondii infection in wild wood mice
Toxoplasma gondii is a highly successful parasite with a worldwide prevalence. Small rodents are the main intermediate hosts, and there is growing evidence that T. gondii modifies their behaviour. Chronically infected rodents show impaired learning capacity, enhanced activity, and, most importantly, a reduction of the innate fear towards cat odour. This modification of host behaviour ensures a successful transmission of T. gondii from rodents to felids, the definitive hosts of the parasite. Given the negative fitness consequences of this behavioural manipulation, as well as an increased mortality during the acute phase of infection, we expect rodents to evolve potent resistance mechanisms that prevent or control infection. Indeed, studies in laboratory mice have identified candidate genes for T. gondii resistance. of particular importance appear to be the innate immune receptors Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12), which recognise T. gondii profilin and initiate immune responses against the parasite. Here we analyse the genetic diversity of TLR11 and TLR12 in a natural population of wood mice (Apodemus sylvaticus), and test for associations between TLR11 and TLR12 polymorphisms and T. gondii infection, as well as for epistatic interactions between TLR11 and TLR12 on infection status. We found that both TLR11 and TLR12 were polymorphic in wood mice, with four and nine amino acid haplotypes, respectively. However, we found no evidence that TLR11 or TLR12 genotypes or haplotypes were significantly associated with Toxoplasma infection. Despite the importance of TLR11 and TLR12 in T. gondii recognition and immune defence initiation, naturally occurring polymorphisms at TLR11 and TLR12 thus appear to play a minor role in mediating qualitative resistance to T. gondii in natural host populations of A. sylvaticus. This highlights the importance of assessing the role of candidate genes for parasite resistance identified in a laboratory setting in an ecologically meaningful context to quantify their role in mediating host-parasite interactions in the wild. © 2014 Elsevier B.V.
Abstract.
Postma E, Siitari H, Schwabl H, Richner H, Tschirren B (2014). The multivariate egg: Quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models.
Oecologia,
174(3), 631-638.
Abstract:
The multivariate egg: Quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models
Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and/or among clutches. Here we tested for such correlations between maternally derived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed-model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed-model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology. © 2013 Springer-Verlag Berlin Heidelberg.
Abstract.
2013
Romero-Diaz C, Richner H, Granado-Lorencio F, Tschirren B, Fitze PS (2013). Independent sources of condition dependency and multiple pathways determine a composite trait: Lessons from carotenoid-based plumage colouration.
Journal of Evolutionary Biology,
26(3), 635-646.
Abstract:
Independent sources of condition dependency and multiple pathways determine a composite trait: Lessons from carotenoid-based plumage colouration
Many colour ornaments are composite traits consisting of at least four components, which themselves may be more complex, determined by independent evolutionary pathways, and potentially being under different environmental control. To date, little evidence exists that several different components of colour elaboration are condition dependent and no direct evidence exists that different ornamental components are affected by different sources of variation. For example, in carotenoid-based plumage colouration, one of the best-known condition-dependent ornaments, colour elaboration stems from both condition-dependent pigment concentration and structural components. Some environmental flexibility of these components has been suggested, but specifically which and how they are affected remains unknown. Here, we tested whether multiple colour components may be condition dependent, by using a comprehensive 3 × 2 experimental design, in which we carotenoid supplemented and immune challenged great tit nestlings (Parus major) and quantified effects on different components of colouration. Plumage colouration was affected by an interaction between carotenoid availability and immune challenge. Path analyses showed that carotenoid supplementation increased plumage saturation via feather carotenoid concentration and via mechanisms unrelated to carotenoid deposition, while immune challenge affected feather length, but not carotenoid concentration. Thus, independent condition-dependent pathways, affected by different sources of variation, determine colour elaboration. This provides opportunities for the evolution of multiple signals within components of ornamental traits. This finding indicates that the selective forces shaping the evolution of different components of a composite trait and the trait's signal content may be more complex than believed so far, and that holistic approaches are required for drawing comprehensive evolutionary conclusions. © 2013 European Society for Evolutionary Biology.
Abstract.
Tschirren B, Andersson M, Scherman K, Westerdahl H, Mittl PRE, Råberg L (2013). Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population.
Proceedings of the Royal Society B: Biological Sciences,
280(1759).
Abstract:
Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population
The discovery of the key role of Toll-like receptors (TLRs) in initiating innate immune responses and modulating adaptive immunity has revolutionized our understanding of vertebrate defence against pathogens. Yet, despite their central role in pathogen recognition and defence initiation, there is little information on how variation in TLRs influences disease susceptibility in natural populations. Here, we assessed the extent of naturally occurring polymorphisms at TLR2 in wild bank voles (Myodes glareolus) and tested for associations between TLR2 variants and infection with Borrelia afzelii, a common tick-transmitted pathogen in rodents and one of the causative agents of human Lyme disease. Bank voles in our population had 15 different TLR2 haplotypes (10 different haplotypes at the amino acid level), which grouped in three well-separated clusters. In a large-scale capture-mark-recapture study, we show that voles carrying TLR2 haplotypes of one particular cluster (TLR2c2) were almost three times less likely to be Borrelia infected than animals carrying other haplotypes. Moreover, neutrality tests suggested that TLR2 has been under positive selection. This is, to our knowledge, the first demonstration of an association between TLR polymorphism and parasitism in wildlife, and a striking example that genetic variation at innate immune receptors can have a large impact on host resistance. © 2013 the Author(s) Published by the Royal Society. All rights reserved.
Abstract.
2012
Tschirren B, Andersson M, Scherman K, Westerdahl H, Råberg L (2012). Contrasting patterns of diversity and population differentiation at the innate immunity gene toll-like receptor 2 (tlr2) in two sympatric rodent species.
Evolution,
66(3), 720-731.
Abstract:
Contrasting patterns of diversity and population differentiation at the innate immunity gene toll-like receptor 2 (tlr2) in two sympatric rodent species
Comparing patterns of diversity and divergence between populations at immune genes and neutral markers can give insights into the nature and geographic scale of parasite-mediated selection. To date, studies investigating such patterns of selection in vertebrates have primarily focused on the acquired branch of the immune system, whereas it remains largely unknown how parasite-mediated selection shapes innate immune genes both within and across vertebrate populations. Here, we present a study on the diversity and population differentiation at the innate immune gene Toll-like receptor 2 (TLR2) across nine populations of yellow-necked mice (Apodemus flavicollis) and bank voles (Myodes glareolus) in southern Sweden. In yellow-necked mice, TLR2 diversity was very low, as was TLR2 population differentiation compared to neutral loci. In contrast, several TLR2 haplotypes co-occurred at intermediate frequencies within and across bank vole populations, and pronounced isolation by distance between populations was observed. The diversity and differentiation at neutral loci was similar in the two species. These results indicate that parasite-mediated selection has been acting in dramatically different ways on a given immune gene in ecologically similar and sympatric species. Furthermore, the finding of TLR2 population differentiation at a small geographical scale in bank voles highlights that vertebrate innate immune defense may be evolutionarily more dynamic than has previously been appreciated. © 2011 the Author(s). Evolution © 2011 the Society for the Study of Evolution.
Abstract.
Tschirren B, Postma E, Rutstein AN, Griffith SC (2012). When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring.
Proc Biol Sci,
279(1731), 1233-1240.
Abstract:
When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring.
Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.
Abstract.
Author URL.
2011
Griffith SC, Pariser EC, Tschirren B, Astheimer LB (2011). Resource allocation across the egg laying sequence in the wild zebra finch Taeniopygia guttata.
Journal of Avian Biology,
42(6), 480-484.
Abstract:
Resource allocation across the egg laying sequence in the wild zebra finch Taeniopygia guttata
Zebra finches have played a central role in the discovery of a variety of maternal effects over the past decade, with females shown to adjust resource allocation to their eggs in response to variables such as the appearance of their partner, their own condition, and the diet on which they are maintained. In addition to being the focus of some of the most high profile individual studies that have influenced maternal effects research in birds, the multitude of zebra finch studies together provide the most comprehensive set of data to illuminate general patterns and compare different maternally derived variables. Surprisingly, to date, virtually all of this work has focused on captive populations of the zebra finch that have been domesticated for many generations, and which are typically held under relatively constant environmental and dietary conditions. Here we report the first data on resource allocation across the egg laying sequence in a free-living wild population. Reassuringly we find that the patterns that have been found in the majority of studies of domesticated populations with respect to investment across the laying sequence were all present in the wild population. The size and mass of eggs increased through the laying sequence whilst the concentration of carotenoids significantly decreased across the laying sequence. Although there was no significant pattern with respect to testosterone across the laying sequence the first two eggs had a higher level of testosterone than the last few eggs in the clutch, which is also consistent with the findings of earlier studies in captive populations. © 2011 the Authors.
Abstract.
Tschirren B, Råberg L, Westerdahl H (2011). Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents.
J Evol Biol,
24(6), 1232-1240.
Abstract:
Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents.
Patterns of selection acting on immune defence genes have recently been the focus of considerable interest. Yet, when it comes to vertebrates, studies have mainly focused on the acquired branch of the immune system. Consequently, the direction and strength of selection acting on genes of the vertebrate innate immune defence remain poorly understood. Here, we present a molecular analysis of selection on an important receptor of the innate immune system of vertebrates, the Toll-like receptor 2 (TLR2), across 17 rodent species. Although purifying selection was the prevalent evolutionary force acting on most parts of the rodent TLR2, we found that codons in close proximity to pathogen-binding and TLR2-TLR1 heterodimerization sites have been subject to positive selection. This indicates that parasite-mediated selection is not restricted to acquired immune system genes like the major histocompatibility complex, but also affects innate defence genes. To obtain a comprehensive understanding of evolutionary processes in host-parasite systems, both innate and acquired immunity thus need to be considered.
Abstract.
Author URL.
2010
Jacot A, Romero-Diaz C, Tschirren B, Richner H, Fitze PS (2010). Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major).
Am Nat,
176(1), 55-62.
Abstract:
Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major).
Carotenoid-based yellowish to red plumage colors are widespread visual signals used in sexual and social communication. To understand their ultimate signaling functions, it is important to identify the proximate mechanism promoting variation in coloration. Carotenoid-based colors combine structural and pigmentary components, but the importance of the contribution of structural components to variation in pigment-based colors (i.e. carotenoid-based colors) has been undervalued. In a field experiment with great tits (Parus major), we combined a brood size manipulation with a simultaneous carotenoid supplementation in order to disentangle the effects of carotenoid availability and early growth condition on different components of the yellow breast feathers. By defining independent measures of feather carotenoid content (absolute carotenoid chroma) and background structure (background reflectance), we demonstrate that environmental factors experienced during the nestling period, namely, early growth conditions and carotenoid availability, contribute independently to variation in yellow plumage coloration. While early growth conditions affected the background reflectance of the plumage, the availability of carotenoids affected the absolute carotenoid chroma, the peak of maximum ultraviolet reflectance, and the overall shape, that is, chromatic information of the reflectance curves. These findings demonstrate that environment-induced variation in background structure contributes significantly to intraspecific variation in yellow carotenoid-based plumage coloration.
Abstract.
Author URL.
Tschirren B, Bensch S (2010). Genetics of personalities: no simple answers for complex traits.
Mol Ecol,
19(4), 624-626.
Abstract:
Genetics of personalities: no simple answers for complex traits.
Identifying the genes that underlie phenotypic variation in natural populations, and assessing the consequences of polymorphisms at these loci for individual fitness are major objectives in evolutionary biology. Yet, with the exception of a few success stories, little progress has been made, and our understanding of the link between genotype and phenotype is still in its infancy. For example, although body length in humans is largely genetically determined, with heritability estimates greater than 0.8, massive genome-wide association studies (GWAS) have only been able to account for a very small proportion of this variation (Gudbjartsson et al. 2008). If it is so difficult to explain the genetics behind relatively 'simple' traits, can we envision that it will at all be possible to find genes underlying complex behavioural traits in wild non-model organisms? Some notable examples suggest that this can indeed be a worthwhile endeavour. Recently, the circadian rhythm gene Clock has been associated with timing of breeding in a wild blue tit population (Johnsen et al. 2007; Liedvogel et al. 2009) and the Pgi gene to variation in dispersal and flight endurance in Glanville fritillary butterflies (Niitepold et al. 2009). A promising candidate gene for influencing complex animal personality traits, also known as behavioural syndromes (Sih et al. 2004), is the dopamine receptor D4 (DRD4) gene. Within the last decade, polymorphisms in this gene have been associated with variation in novelty seeking and exploration behaviour in a range of species, from humans to great tits (Schinka et al. 2002; Fidler et al. 2007). In this issue, Korsten et al. (2010) attempt to replicate this previously observed association in wild-living birds, and test for the generality of the association between DRD4 and personality across a number of European great tit populations.
Abstract.
Author URL.
Tschirren B, Postma E (2010). Quantitative genetics research in Zebra Finches: Where we are and where to go.
Emu,
110(3), 268-278.
Abstract:
Quantitative genetics research in Zebra Finches: Where we are and where to go
The ease with which Zebra Finches can be kept and bred in captivity makes them a suitable model for avian quantitative genetic studies. After a brief introduction to some quantitative genetic concepts, we here provide an up-to-date overview of quantitative genetic studies in Zebra Finches. We discuss what these studies can teach us about the evolutionary and behavioural ecology of Zebra Finches and song birds in general, and make suggestions for future research. Throughout this article we plead for a greater appreciation of the advantages offered by working on captive birds, but also discuss their limitations. Although quantitative genetic analyses in natural populations are becoming increasingly powerful, these studies lack the control possible in captivity. However, obtaining meaningful estimates of the type and strength of selection acting on phenotypic variation is more difficult in captivity. Hence, quantitative genetic studies in the wild and captivity each have their strengths and weaknesses and should be considered complementary rather than opposing. However, whereas quantitative genetic studies in the wild have boomed, the unique advantages offered by captive Zebra Finches have remained underexploited. Here we make a first attempt at changing this by highlighting what we believe may be fruitful lines for future research. © 2010 Royal Australasian Ornithologists Union.
Abstract.
2009
Tschirren B, Sendecka J, Groothuis TGG, Gustafsson L, Doligez B (2009). Heritable variation in maternal yolk hormone transfer in a wild bird population.
Am Nat,
174(4), 557-564.
Abstract:
Heritable variation in maternal yolk hormone transfer in a wild bird population.
Differential reproductive investment by the mother can critically influence offspring development and phenotype, and strong selection is therefore expected to act on such maternal effects. Although a genetic basis is a prerequisite for phenotypic traits to respond to selection and thus to evolve, we still know very little about the extent of heritable variation in maternal effects in natural populations. Here, we present the first estimates of intrafemale repeatability across breeding seasons and estimates of heritability of hormone-mediated maternal effects in a wild population of collared flycatchers (Ficedula albicollis). We found that maternal yolk testosterone (T) concentrations, yolk mass, and egg mass were moderately to highly repeatable within females across years, whereas intrafemale consistency of maternal yolk androstenedione (A4) deposition was low yet statistically significant. Furthermore, maternal yolk T transfer, yolk mass, and egg mass were significantly heritable, whereas yolk A4 transfer was not. These results strongly suggest that two major maternal yolk androgens are differentially regulated by genes and the environment. Selection on heritable variation in maternal yolk T deposition has the potential to shape the rate and direction of phenotypic change in offspring traits and can thereby accelerate or impede the response to selection in natural populations.
Abstract.
Author URL.
Bischoff LL, Tschirren B, Richner H (2009). Long-term effects of early parasite exposure on song duration and singing strategy in great tits.
Behavioral Ecology,
20(2), 265-270.
Abstract:
Long-term effects of early parasite exposure on song duration and singing strategy in great tits
Song is a sexually selected trait in many bird species and has been suggested to function as a signal of a male's health and parasite resistance. Here we present an experimental field study on the long-term effects of parasite exposure early in life on adult bird song. We exposed nestling great tits (Parus major) to ectoparasitic hen fleas (Ceratophyllus gallinae) and on their recruitment into the local breeding population assessed the response to a playback of a challenging male in their breeding territory. We show, to our knowledge for the first time in a wild bird population, that parasite exposure early in life affects bird song: song duration of males that were exposed to parasites early in life was reduced by 32% compared with males that grew up in a flea-free environment. Early parasite exposure also significantly reduced the degree of song overlap with the playback, which has been shown to correlate with social status. There was no effect of early parasite exposure on the number of different song types sung or on the latency until the males started the vocal response to the playback. These results suggest that mates or rivals can use song duration and song overlap as proxies for an individual's exposure to parasites early in life. It thereby highlights both the importance of parasites in maintaining honesty of sexually selected traits and the costs of parasitism in terms of reduced attractiveness and competitiveness.
Abstract.
Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009). Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches.
J Evol Biol,
22(2), 387-395.
Abstract:
Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches.
Divergent selection pressures among populations can result not only in significant differentiation in morphology, physiology and behaviour, but also in how these traits are related to each other, thereby driving the processes of local adaptation and speciation. In the Australian zebra finch, we investigated whether domesticated stock, bred in captivity over tens of generations, differ in their response to a life-history manipulation, compared to birds taken directly from the wild. In a 'common aviary' experiment, we thereto experimentally manipulated the environmental conditions experienced by nestlings early in life by means of a brood size manipulation, and subsequently assessed its short- and long-term consequences on growth, ornamentation, immune function and reproduction. As expected, we found that early environmental conditions had a marked effect on both short- and long-term morphological and life-history traits in all birds. However, although there were pronounced differences between wild and domesticated birds with respect to the absolute expression of many of these traits, which are indicative of the different selection pressures wild and domesticated birds were exposed to in the recent past, manipulated rearing conditions affected morphology and ornamentation of wild and domesticated finches in a very similar way. This suggests that despite significant differentiation between wild and domesticated birds, selection has not altered the relationships among traits. Thus, life-history strategies and investment trade-offs may be relatively stable and not easily altered by selection. This is a reassuring finding in the light of the widespread use of domesticated birds in studies of life-history evolution and sexual selection, and suggests that adaptive explanations may be legitimate when referring to captive bird studies.
Abstract.
Author URL.
Pitala N, Ruuskanen S, Laaksonen T, Doligez B, Tschirren B, Gustafsson L (2009). The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis.
Journal of Avian Biology,
40(2), 225-230.
Abstract:
The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis
Hormone-mediated maternal effects may be an important mechanism for adjusting offspring phenotype to particular requirements of the environment. We manipulated the levels of testosterone and androstenedione in the yolk of collared flycatcher Ficedula albicollis eggs to investigate the effects of pre-natal exposure to androgens on growth and immune function. Androgen treatment tended to reduce the growth of males, and enhance the growth of females, as indicated by significant interaction between sex and androgen treatment. Cellular immune function was not affected by androgen treatment or sex. Survival of nestlings until fledging was not related to androgen treatment. Our results indicate that in the collared flycatcher yolk androgens do not involve clear overall benefits during the nestling stage, and that growth-enhancing effects of increased yolk androgen levels on female nestlings are counterbalanced by detrimental effects on male nestlings. © 2009 the Authors.
Abstract.
Tschirren B, Siitari H, Saladin V, Richner H (2009). Transgenerational immunity in a bird-ectoparasite system: Do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas?.
Ibis,
151(1), 160-170.
Abstract:
Transgenerational immunity in a bird-ectoparasite system: Do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas?
During egg formation, female birds deposit antibodies against parasites and pathogens they were exposed to before egg laying into the yolk. In captive bird species, it has been shown that these maternal immunoglobulins (maternal yolk IgGs) can protect newly hatched offspring against infection. However, direct evidence for such benefits in wild birds is hitherto lacking. We investigated (1) if nestling Great Tits Parus major originating from eggs with naturally high levels of maternal yolk IgG are less susceptible to a common, nest-based ectoparasite, (2) if maternal yolk IgGs influence nestling development and in particular, their own immune defence, and (3) if there is a negative correlation between levels of maternal yolk IgG in host eggs and the reproductive success of ectoparasitic fleas feeding on the nestlings. Counter to expectations, we found no indication that maternally transferred yolk IgGs have direct beneficial effects on nestling development, nestling immune response or nestling resistance or tolerance to fleas. Furthermore, we found no negative correlation between host yolk IgG levels and parasite fecundity. Thus, whereas previous work has unequivocally shown that prenatal maternal effects play a crucial role in shaping the parasite resistance of nestling birds, our study indicates that other egg components, such as hormones, carotenoids or other immuno-active substances, which bird females can adjust more quickly than yolk IgG, might mediate these effects. © 2008 the Authors.
Abstract.
Ruuskanen S, Doligez B, Tschirren B, Pitala N, Gustafsson L, Groothuis TGG, Laaksonen T (2009). Yolk androgens do not appear to mediate sexual conflict over parental investment in the collared flycatcher Ficedula albicollis.
Horm Behav,
55(4), 514-519.
Abstract:
Yolk androgens do not appear to mediate sexual conflict over parental investment in the collared flycatcher Ficedula albicollis.
Males and females are in conflict over parental care, as it would be favourable for one parent to shift labour to the other. Yolk hormones may offer a mechanism through which female birds could influence offspring traits in ways that increase the relative investment by the male. We studied the role of yolk androgens in mediating sexual conflict over parental care in the collared flycatcher (Ficedula albicollis). In a cross-fostering experiment, the male's proportion of total feeding visits increased with increasing androgen levels in the foster eggs. This could suggest that sexual conflict over parental care may be influenced by the female's differential allocation of yolk androgens or a maternal effect associated with yolk androgens. However, when we experimentally elevated yolk androgen levels, male feeding rates did not differ between control and androgen-manipulated nests. This suggests that other egg components correlated with yolk androgen levels, rather than yolk androgen levels per se, may influence male parental effort. In conclusion, yolk androgens per se do not appear to mediate sexual conflict over parental investment in the collared flycatcher.
Abstract.
Author URL.
2008
Tschirren B, Richner H (2008). Differential effects of yolk hormones on maternal and paternal contribution to parental care.
Animal Behaviour,
75(6), 1989-1994.
Abstract:
Differential effects of yolk hormones on maternal and paternal contribution to parental care
In species with biparental care, a female gains fitness benefits from the joint reproductive investment of herself and her partner, but pays only the costs of her own care. Selection thus favours mechanisms that allow females to elicit a higher paternal investment from their partners. In oviparous species, the allocation of maternal yolk androgens to the eggs might represent such a female adaptation to sexually antagonistic selection. To test this hypothesis, we experimentally blocked the effects of maternal yolk androgens by an injection of the antiandrogen flutamide or a control substance in the eggs of great tits, Parus major. We subsequently manipulated the food demand of the brood in a brood size manipulation experiment, and recorded the parental feeding rates. The males' food-provisioning rates were not significantly influenced by the actions of maternal yolk androgens, whereas females adjusted their parental effort to androgen-mediated nestling signals, in particular in enlarged broods. These results show that female great tits do not exploit the male's contribution to parental care by allocating high concentrations of yolk androgens to their eggs. However, they indicate that variation in yolk androgen allocation among females has evolved through a process of coadaptation that matches maternal food provisioning and offspring demand. © 2008 the Association for the Study of Animal Behaviour.
Abstract.
2007
Fitze PS, Tschirren B, Gasparini J, Richner H (2007). Carotenoid-based plumage colors and immune function: is there a trade-off for rare carotenoids?.
Am Nat,
169 Suppl 1, S137-S144.
Abstract:
Carotenoid-based plumage colors and immune function: is there a trade-off for rare carotenoids?
Theory suggests that carotenoid-based signals are used in animal communication because they contain specific information about parasite resistance or immunocompetence. This implies that honesty of carotenoid-based signals is maintained by a trade-off between pigmentation and immune function for carotenoids, assuming that the carotenoids used for coloration are also immunoenhancing. We tested this hypothesis by altering the diets of nestling great tits (Parus major) with supplementary beadlets containing the carotenoids that are naturally ingested with food or beadlets containing the carotenoids that are incorporated into the feathers; a control group received beadlets containing no carotenoids. We simultaneously immune challenged half of the nestlings of each supplementation group, using a two-factorial design. Activation of the immune system led to reduced color expression. However, only nestlings fed with the naturally ingested carotenoids and not with the carotenoids deposited in the feathers showed an increased cellular immune response. This shows that the carotenoids used for ornamentation do not promote the immune function, which conflicts with the trade-off hypothesis. Our results indicate that honesty of carotenoid-based signals is maintained by an individual's physiological limitation to absorb and/or transport carotenoids and by access to carotenoids, indicating that preferences for carotenoid-based traits in sexual selection or parent-offspring interactions select for competitive individuals, rather than specifically for immune function.
Abstract.
Author URL.
Tschirren B, Bischoff LL, Saladin V, Richner H (2007). Host condition and host immunity affect parasite fitness in a bird-ectoparasite system.
Functional Ecology,
21(2), 372-378.
Abstract:
Host condition and host immunity affect parasite fitness in a bird-ectoparasite system
1. Parasites might preferentially feed on hosts in good nutritional condition as such hosts provide better resources for the parasites' own growth, survival and reproduction. However, hosts in prime condition are also better able to develop costly immunological or physiological defence mechanisms, which in turn reduce the parasites' reproductive success. The interplay between host condition, host defence and parasite fitness will thus play an important part in the dynamics of host-parasite systems. 2. In a 2 × 2 design, we manipulated both the access to food in great tit Parus major broods and the exposure of the nestlings to hen fleas Ceratophyllus gallinae, a common ectoparasite of hole-breeding birds. We subsequently investigated the role of manipulated host condition, host immunocompetence, and experimentally induced host defence in nestlings on the reproductive success of individual hen flea females. 3. The food supplementation of the nestlings significantly influenced the parasites' reproductive success. Female fleas laid significantly more eggs when feeding on food-supplemented hosts. 4. Previous parasite exposure of the birds affected the reproductive success of fleas. However, the impact of this induced host response on flea reproduction depended on the birds' natural level of immunocompetence, assessed by the phytohaemagglutinin (PHA) skin test. Flea fecundity significantly decreased with increasing PHA response of the nestlings in previously parasite-exposed broods. No relationship between flea fitness and host immunocompetence was, however, found in previously unexposed broods. The PHA response thus correlates with the nestlings' ability to mount immunological or physiological defence mechanisms against hen fleas. No significant interaction effect between early flea exposure and food supplementation on the parasites' reproductive success was found. 5. Our study shows that the reproductive success of hen fleas is linked to the hosts' food supply early in life and their ability to mount induced immunological or physiological defence mechanisms. These interactions between host quality and parasite fitness are likely to influence host preference, host choice and parasite virulence and thus the evolutionary dynamics in host-parasite systems. © 2007 the Authors.
Abstract.
Tschirren B, Fitze PS, Richner H (2007). Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism?.
Am Nat,
169(1), 87-93.
Abstract:
Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism?
The decision of how far to disperse from the natal territory has profound and long-lasting consequences for young animals, yet the optimal dispersal behavior often depends on environmental factors that are difficult or impossible to assess by inexperienced juveniles. Natural selection thus favors mechanisms that allow the adaptive and flexible adjustment of the offspring's dispersal behavior by their parents via either paternal or maternal effects. Here we show that different dispersal strategies maximize the reproductive success of young great tits (Parus major) originating from a parasite-infested or a parasite-free nest and demonstrate that differential transfer of maternal yolk androgens in response to parasitism can result in a modification of the offspring's dispersal behavior that appears adaptive. It demonstrates that prenatal maternal effects are an important yet so far neglected determinant of natal dispersal and highlights the potential importance of maternal effects in mediating coevolutionary processes in host-parasite systems.
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Author URL.
2006
Fitze PS, Tschirren B (2006). No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major).
J Evol Biol,
19(2), 618-624.
Abstract:
No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major).
In several vertebrate species evidence supports the hypothesis that carotenoid-based coloration of adults has evolved due to sexual selection. However, in some birds already the nestlings display carotenoid-based coloration. Because the nestling's body plumage is typically moulted before the first reproductive event, sexual selection cannot explain the evolution of these carotenoid-based traits. This suggests that natural selection might be the reason for its evolution. Here we test whether the carotenoid-based nestling coloration of great tits (Parus major) predicts survival after fledging. Contrary to our expectation, the carotenoid-based plumage coloration was not related to short- nor to long-term survival in the studied population. Additionally, no prefledging selection was detectable in an earlier study. This indicates that the carotenoid-based coloration of nestling great tits is currently not under natural selection and it suggests that past selection pressures or selection acting on correlated traits may have led to its evolution.
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Author URL.
Tschirren B, Richner H (2006). Parasites shape the optimal investment in immunity.
Proc Biol Sci,
273(1595), 1773-1777.
Abstract:
Parasites shape the optimal investment in immunity.
The evolution of optimal functioning and maintenance of the immune system is thought to be driven by the costs arising from the allocation of resources to immune functions rather than to growth and reproduction and by the benefits arising from higher defence if an infection occurs. In young animals there is a high premium for fast growth and competitiveness and a parasite-mediated trade-off is thus predicted between the allocation of resources to growth versus immune function. In a field study on nestling great tits (Parus major), we manipulated simultaneously the level of immune defence by a dietary supplementation of the immunostimulant methionine and ectoparasite (Ceratophyllus gallinae) abundance in the nest and thereby assessed both the costs and benefits of investing in immune defence. Nestlings supplemented with methionine grew slower during the experimental boost of their immune system compared to controls. Thereafter, however, nestlings with a boosted immune system grew at faster rates under parasite pressure compared to unstimulated birds. It experimentally shows the costs and benefits of investment in immunity and suggests that the evolution of optimum host defence is governed by a parasite-mediated allocation trade-off between growth and immune function.
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Author URL.
2005
Tschirren B, Fitze PS, Richner H (2005). Carotenoid-based nestling colouration and parental favouritism in the great tit.
Oecologia,
143(3), 477-482.
Abstract:
Carotenoid-based nestling colouration and parental favouritism in the great tit.
While elaborate carotenoid-based traits in adult birds may have evolved as honest signals of individual quality in the context of sexual selection or other social interactions, the function of carotenoid-based colours in juveniles is less well understood. We investigated the hypothesis that carotenoid-based nestling colouration has evolved in response to parental preference of intensely coloured offspring during food provisioning. In a field experiment, we manipulated nestling plumage colouration by a carotenoid-supplementation and analysed the parental food provisioning behaviour before feather appearance and at the end of the nestling stage. Carotenoids per se did not influence the nestling's begging behaviour or parental feeding decisions and we found no evidence that carotenoid-based colouration in nestling great tits has a signalling function in parent-offspring interactions. Parents did not discriminate between intensely coloured and control offspring in their food provisioning and in accordance with this finding intensely coloured nestlings were not heavier or larger at the end of the nestling stage. Alternative explanations for the evolution of carotenoid-based colours in nestling birds are discussed.
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Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005). Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings.
Journal of Animal Ecology,
74(4), 675-682.
Abstract:
Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings
1. Maternal yolk hormones can enhance the development and phenotypic quality of nestling birds. Nevertheless, within species large differences in yolk androgen concentrations among clutches are observed. This differential allocation of maternal yolk hormones might be explained by a trade-off between beneficial effects of yolk androgens and their associated costs. 2. Potential costs include an increased susceptibility to parasites in nestlings exposed to high concentrations of yolk androgens during embryonic development, weaker immune response or increased levels of circulating corticosterone that indirectly reduce immune function. 3. In a field study, we manipulated yolk testosterone in great tit (Parus major) eggs and tested the nestling's susceptibility to ectoparasites as measured by the parasites' effect on growth, the cellular immune response, and the levels of circulating corticosterone. 4. At the end of the nestling period, nestlings originating from testosterone-injected eggs were heavier than control nestlings. This effect was strongest in nestlings at the end of the size hierarchy, as shown by a significant interaction between hormone treatment and the nestlings' size rank within nests. 5. High levels of yolk testosterone promoted growth of the nestling's body mass similarly in parasite-infested and parasite-free nests, and neither affected the levels of plasma corticosterone, nor the nestling's cell-mediated immune response. 6. In summary, our results do not show negative short-term effects of high concentrations of yolk testosterone on immune function or parasite susceptibility, but emphasize that maternal investment via deposition of yolk testosterone can promote fitness-related growth and development of nestlings. © 2005 British Ecological Society.
Abstract.
2004
Tschirren B, Richner H, Schwabl H (2004). Ectoparasite-modulated deposition of maternal androgens in great tit eggs.
Proc Biol Sci,
271(1546), 1371-1375.
Abstract:
Ectoparasite-modulated deposition of maternal androgens in great tit eggs.
Maternal yolk androgens can promote growth and competitive abilities of nestling birds but are also suggested to increase susceptibility to parasites or suppress immune function. We tested the hypothesis that females exposed to ectoparasites during egg formation will adjust the content of androgens in the yolk. We predicted that when anticipating high levels of parasitism, females deposit (i) less androgens into all eggs of their clutch and (ii) smaller amounts of androgens in eggs late in the laying sequence to facilitate brood reduction. In a field experiment we exposed female great tits (Parus major) to hen fleas (Ceratophyllus gallinae), or kept them free of ectoparasites prior to egg laying. We collected the eggs and measured yolk concentrations of androstenedione (A4), testosterone (T) and 5alpha-dihydrotestosterone (DHT) by radioimmunoassay. Among clutches, eggs of ectoparasite-exposed females contained significantly less A4 and tended to contain less T, whereas DHT content was unaffected. Within clutches, content of A4 and T increased significantly with laying order whereas DHT content significantly decreased. These patterns were unaffected by ectoparasites. In summary, our results provide no evidence for hormone-based facilitation of brood reduction under ectoparasite exposure but support the hypothesis that females exposed to ectoparasites reduce levels of T and its precursor A4 in yolk and might thereby reduce the negative effects of parasites on offspring.
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Author URL.
Fitze PS, Tschirren B, Richner H (2004). Life history and fitness consequences of ectoparasites.
Journal of Animal Ecology,
73(2), 216-226.
Abstract:
Life history and fitness consequences of ectoparasites
1. For iteroparous organisms life-history theory predicts a trade-off between current and future reproduction, and therefore the evolution of host responses to current parasite infestation that will maximize lifetime reproductive success. The parasite-induced variation in reproductive success is thus not the net result of parasite infestation alone, but the parasite-mediated outcome of optimal resource allocation among current and future reproductive events. Understanding the importance of parasites for the evolution of host life history therefore requires an experimental investigation of the effects of parasites over the host's life span. Such studies are currently scant. 2. We manipulated the load of an ectoparasite, the hen flea (Ceratophyllus gallinae), in the nests of its most common host, the great tit (Parus major), over a period of 4 years and recorded, the components of current and future reproductive success including survival, divorce, breeding dispersal and various reproductive parameters. Finally we assessed, for females only as paternity of males was unknown, the lifetime reproductive success as a close correlate of Darwinian fitness. 3. For current reproduction, our experiment demonstrates that parasites reduce current reproductive success via an increase in the probability of nest failure during incubation and the nestling period. In the presence of fleas, clutch size and the number of fledglings were reduced while the incubation and the nestling period were prolonged. Thus parasitism led to an increase in parental effort but nevertheless reduced current reproductive success. 4. For future reproduction, the experiment shows that females breeding in infested nests dispersed over longer distances between breeding attempts. The divorce rate following infestation, the probability of breeding locally in the future and residual reproductive success were not affected significantly by ectoparasites. The study thus suggests that hen fleas play a minor role in shaping the trade-off between current and future reproduction. 5. Lifetime reproductive success of females, measured as the total number of locally recruiting offspring over the 4 experimental years, was reduced significantly by ectoparasites. The negative effect of parasites arose by a reduction of the number of fledglings per breeding attempt rather than by a reduction of the number of breeding attempts.
Abstract.
Tschirren B, Fitze PS, Richner H (2004). Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings (vol 72, pg 839, 2003).
JOURNAL OF ANIMAL ECOLOGY,
73(4), 814-814.
Author URL.
2003
Fitze PS, Tschirren B, Richner H (2003). Carotenoid-based colour expression is determined early in nestling life.
Oecologia,
137(1), 148-152.
Abstract:
Carotenoid-based colour expression is determined early in nestling life.
Carotenoid-based colours are widespread in animals and are used as signals in intra- and interspecific communication. In nestling birds, the carotenoids used for feather pigmentation may derive via three pathways: (1) via maternal transfer to egg yolk; (2) via paternal feeds early after hatching when females are mainly brooding; or (3) via feeds from both parents later in nestling life. We analysed the relative importance of the proposed carotenoid sources in a field experiment on great tit nestlings ( Parus major). In a within-brood design we supplemented nestlings with carotenoids shortly after hatching, later on in the nestling life, or with a placebo. We show that the carotenoid-based colour expression of nestlings is modified maximally during the first 6 days after hatching. It reveals that the observed variation in carotenoid-based coloration is based only on mechanisms acting during a short period of time in early nestling life. The experiment further suggests that paternally derived carotenoids are the most important determinants of nestling plumage colour.
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Author URL.
Tschirren B, Fitze PS, Richner H (2003). Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.).
J Evol Biol,
16(1), 91-100.
Abstract:
Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.).
Many vertebrates use carotenoid-based signals in social or sexual interactions. Honest signalling via carotenoids implies some limitation of carotenoid-based colour expression among phenotypes in the wild, and at least five limiting proximate mechanisms have been hypothesized. Limitation may arise by carotenoid-availability, genetic constraints, body condition, parasites, or detrimental effects of carotenoids. An understanding of the relative importance of the five mechanisms is relevant in the context of natural and sexual selection acting on signal evolution. In an experimental field study with carotenoid supplementation, simultaneous cross-fostering, manipulation of brood size and ectoparasite load, we investigated the relative importance of these mechanisms for the variation in carotenoid-based coloration of nestling great tits (Parus major). Carotenoid-based plumage coloration was significantly related to genetic origin of nestlings, and was enhanced both in carotenoid-supplemented nestlings, and nestlings raised in reduced broods. We found a tendency for ectoparasite-induced limitation of colour expression and no evidence for detrimental effects of carotenoids on growth pattern, mortality and recruitment of nestlings to the local breeding population. Thus, three of the five proposed mechanisms can generate individual variation in the expression of carotenoid-based plumage coloration in the wild and thus could maintain honesty in a trait potentially used for signalling of individual quality.
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Author URL.
Tschirren B, Fitze PS, Richner H (2003). Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings.
Journal of Animal Ecology,
72(5), 839-845.
Abstract:
Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings
1. Parasites can affect host fitness, provoke host responses, and thereby mediate host life history evolution. As life history strategies are often sex-specific, immunological or behavioural responses of the host aiming to reduce the impact of parasites may be sexually dimorphic, e.g. as a consequence of sex differences in the resource allocation trade-off between parasite defence, morphological traits and body functions. Parasites may therefore affect males and females differently leading to sex specific patterns of parasite susceptibility. 2. In an experimental field study, we manipulated the ectoparasite load of great tit nests (Parus major) and investigated its effects on male and female nestlings. As susceptibility to parasites may be linked to the ability of the nestlings to fight off parasites immunologically, we further investigated sex differences in cell-mediated immunity using a phytohaemagglutinin (PHA) assay. 3. Body mass, metatarsus length and overall body size, but not feather length, showed a sexual dimorphism at the end of the nestling period. A significant interaction between the effects of sex and parasite treatment on the sexually dimorphic traits indicates that the parasite effect is sex-specific. While no differences in morphological traits were found in females raised in infested and uninfested nests, parasitized males were significantly smaller and lighter than males raised in uninfested nests. Further, we found a pronounced sexual dimorphism in the response to the PHA assay with males showing a reduced cellular immunity. The parasite treatment had a non-significant effect on the PHA response and the PHA response of males and females were not influenced differently by parasites. 4. Our study shows that sexual dimorphism in susceptibility to parasites and immunocompetence develops early in life, and suggests sex-specific strategies in the allocation of limited resources. Possible mechanisms of sex differences in susceptibility to parasites and immunocompetence during postnatal growth and the consequences for optimal sex allocation strategies of the parents are discussed.
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