Publications by year
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 Full text.
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 Full text.
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.
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Tschirren B, Romero Haro AA, Zahn S, Criscuolo F (2020). Sex-specific effects of experimental ectoparasite infestation on telomere length in great tit nestlings.
Journal of Evolutionary Biology Full text.
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 Full text.
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.
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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 Full text.
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.
Evolution Letters Full text.
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.
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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.
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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.
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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?
© 2017 European Society for Evolutionary Biology. Journal of Evolutionary Biology © 2017 European Society for Evolutionary Biology 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
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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.
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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.
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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.
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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
© 2016 the Author(s) Published by the Royal Society. All rights reserved. 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.
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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
© 2016 the Author(s). 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.
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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
© 2016 by the University of Chicago. 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.
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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
© 2016, Nature Publishing Group. All rights reserved. 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.
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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.
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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
© 2016 the Linnean Society of London. 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.
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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
© 2016 Official journal of the Genetics Society. 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.
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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.
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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.
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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
© 2015 the Author(s) Published by the Royal Society. All rights reserved. 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.
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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?
© 2015 Barbara Tschirren. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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.
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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.
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Distinct haplotype structure at the innate immune receptor Toll-like receptor 2 across bank vole populations and lineages in Europe
© 2015 the Linnean Society of London. 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.
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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
© 2015, Springer-Verlag Berlin Heidelberg. 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.
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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.
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Sex-specific effects of prenatal and postnatal nutritional conditions on the oxidative status of great tit nestlings
© 2014, Springer-Verlag Berlin Heidelberg. 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.
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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
© 2014 International Society for Behavioral Ecology. All rights reserved. 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.
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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
© 2014 John Wiley. &. Sons Ltd/CNRS. 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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Author URL.
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.
Abstract.