Adult telomere length is positively correlated with survival and lifetime reproductive success in a wild passerine.

Explaining variation in individual fitness is a key goal in evolutionary biology. Recently, telomeres, repeating DNA sequences capping chromosome ends, have gained attention as a biomarker for body state, physiological costs, and senescence. Existing research has provided mixed evidence for whether telomere length correlates with fitness, including survival and reproductive output. Moreover, few studies have examined how the rate of change in telomere length correlates with fitness in wild populations. Here, we intensively monitored an insular population of house sparrows, and collected longitudinal telomere and life history data (16 years, 1225 individuals). We tested whether telomere length and its rate of change predict fitness measures, namely survival, lifespan and annual and lifetime reproductive effort and success. Telomere length positively predicted short-term survival, independent of age, but did not predict lifespan, suggesting either a diminishing telomere length-survival correlation with age or other extrinsic factors of mortality. The positive association of telomere length with survival translated into reproductive benefits, as birds with longer telomeres produced more genetic recruits, hatchlings and reared more fledglings over their lifetime. In contrast, there was no association between telomere dynamics and annual reproductive output, suggesting telomere dynamics might not reflect the costs of reproduction in this population, potentially masked by variation in individual quality. The rate of change of telomere length did not correlate with neither lifespan nor lifetime reproductive success. Our results provide further evidence that telomere length correlates with fitness, and contribute to our understanding of the selection on, and evolution of, telomere dynamics.

Longitudinal gut microbiome dynamics in relation to age and senescence in a wild animal population.

In humans, gut microbiome (GM) differences are often correlated with, and sometimes causally implicated in, ageing. However, it is unclear how these findings translate in wild animal populations. Studies that investigate how GM dynamics change within individuals, and with declines in physiological condition, are needed to fully understand links between chronological age, senescence and the GM, but have rarely been done. Here, we use longitudinal data collected from a closed population of Seychelles warblers (Acrocephalus sechellensis) to investigate how bacterial GM alpha diversity, composition and stability are associated with host senescence. We hypothesised that GM diversity and composition will differ, and become more variable, in older adults, particularly in the terminal year prior to death, as the GM becomes increasingly dysregulated due to senescence. However, GM alpha diversity and composition remained largely invariable with respect to adult age and did not differ in an individual's terminal year. Furthermore, there was no evidence that the GM became more heterogenous in senescent age groups (individuals older than 6 years), or in the terminal year. Instead, environmental variables such as season, territory quality and time of day, were the strongest predictors of GM variation in adult Seychelles warblers. These results contrast with studies on humans, captive animal populations and some (but not all) studies on non-human primates, suggesting that GM deterioration may not be a universal hallmark of senescence in wild animal species. Further work is needed to disentangle the factors driving variation in GM-senescence relationships across different host taxa.

Causes and consequences of telomere lengthening in a wild vertebrate population.

Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening - an apparent increase in telomere length between repeated samples from the same individual - also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening - which occurs in adults of this species - is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e., low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e., high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres - indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over an individuals lifetime.

Telomere heritability and parental age at conception effects in a wild avian population.

Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. Heritability of telomere length has primarily been calculated using parent-offspring regression which can be confounded by shared environments. To control for confounding variables, quantitative genetic "animal models" can be used, but few studies have applied animal models in wild populations. Furthermore, parental age at conception may also influence offspring telomere length, but most studies have been cross-sectional. We investigated within- and between-parental age at conception effects and heritability of telomere length in the Seychelles warbler using measures from birds caught over 20 years and a multigenerational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). Animal models provided evidence that heritability and evolvability of telomere length were low in this population, and that variation in telomere length was not driven by early-life effects of hatch period or parental identities. Quantitative polymerase chain reaction plate had a large influence on telomere length variation and not accounting for it in the models would have underestimated heritability. Our study illustrates the need to include and account for technical variation in order to accurately estimate heritability, as well as other environmental effects, on telomere length in natural populations.

Early-life seasonal, weather and social effects on telomere length in a wild mammal.

Early-life environmental conditions can provide a source of individual variation in life-history strategies and senescence patterns. Conditions experienced in early life can be quantified by measuring telomere length, which can act as a biomarker of survival probability in some species. Here, we investigate whether seasonal changes, weather conditions and group size are associated with early-life and/or early-adulthood telomere length in a wild population of European badgers (Meles meles). We found substantial intra-annual changes in telomere length during the first 3 years of life, where within-individual effects showed shorter telomere lengths in the winter following the first spring and a trend for longer telomere lengths in the second spring compared to the first winter. In terms of weather conditions, cubs born in warmer, wetter springs with low rainfall variability had longer early-life (3-12 months old) telomeres. Additionally, cubs born in groups with more cubs had marginally longer early-life telomeres, providing no evidence of resource constraint from cub competition. We also found that the positive association between early-life telomere length and cub survival probability remained when social and weather variables were included. Finally, after sexual maturity, in early adulthood (i.e., 12-36 months) we found no significant association between same-sex adult group size and telomere length (i.e., no effect of intrasexual competition). Overall, we show that controlling for seasonal effects, which are linked to food availability, is important in telomere length analyses, and that variation in telomere length in badgers reflects early-life conditions and also predicts first year cub survival.

Contemporary evolution of the innate immune receptor gene TLR3 in an isolated vertebrate population.

Understanding where genetic variation exists, and how it influences fitness within populations is important from an evolutionary and conservation perspective. Signatures of past selection suggest that pathogen-mediated balancing selection is a key driver of immunogenetic variation, but studies tracking contemporary evolution are needed to help resolve the evolutionary forces and mechanism at play. Previous work in a bottlenecked population of Seychelles warblers (Acrocephalus sechellensis) show that functional variation has been maintained at the viral-sensing Toll-like receptor 3 (TLR3) gene, including one nonsynonymous SNP, resulting in two alleles. Here, we characterise evolution at this TLR3 locus over a 25-year period within the original remnant population of the Seychelles warbler, and in four other derived, populations. Results show a significant and consistent temporal decline in the frequency of the TLR3C allele in the original population, and that similar declines in the TLR3C allele frequency occurred in all the derived populations. Individuals (of both sexes) with the TLR3CC genotype had lower survival, and males - but not females - that carry the TLR3C allele had significantly lower lifetime reproductive success than those with only the TLR3A allele. These results indicate that positive selection on the TLR3A allele, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warbler. No evidence of heterozygote advantage was detected. However, whether the positive selection observed is part of a longer-term pattern of balancing selection (through fluctuating selection or rare-allele advantage) cannot be resolved without tracking the TLR3C allele over an extended time period.

Estimation of environmental, genetic and parental age at conception effects on telomere length in a wild mammal.

Understanding individual variation in fitness-related traits requires separating the environmental and genetic determinants. Telomeres are protective caps at the ends of chromosomes that are thought to be a biomarker of senescence as their length predicts mortality risk and reflect the physiological consequences of environmental conditions. The relative contribution of genetic and environmental factors to individual variation in telomere length is, however, unclear, yet important for understanding its evolutionary dynamics. In particular, the evidence for transgenerational effects, in terms of parental age at conception, on telomere length is mixed. Here, we investigate the heritability of telomere length, using the 'animal model', and parental age at conception effects on offspring telomere length in a wild population of European badgers (Meles meles). Although we found no heritability of telomere length and low evolvability (<0.001), our power to detect heritability was low and a repeatability of 2% across individual lifetimes provides a low upper limit to ordinary narrow-sense heritability. However, year (32%) and cohort (3%) explained greater proportions of the phenotypic variance in telomere length, excluding qPCR plate and row variances. There was no support for cross-sectional or within-individual parental age at conception effects on offspring telomere length. Our results indicate a lack of transgenerational effects through parental age at conception and a low potential for evolutionary change in telomere length in this population. Instead, we provide evidence that individual variation in telomere length is largely driven by environmental variation in this wild mammal.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Allelic diversity and patterns of selection at the major histocompatibility complex class I and II loci in a threatened shorebird, the Snowy Plover (Charadrius nivosus).

BACKGROUND: Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classical MHC genes show high polymorphism and are under strong balancing selection, as their products trigger the adaptive immune response in vertebrates. Here, we assess the allelic diversity and patterns of selection for MHC class I and class II loci in a threatened shorebird with highly flexible mating and parental care behaviour, the Snowy Plover (Charadrius nivosus) across its broad geographic range. RESULTS: We determined the allelic and nucleotide diversity for MHC class I and class II genes using samples of 250 individuals from eight breeding population of Snowy Plovers. We found 40 alleles at MHC class I and six alleles at MHC class II, with individuals carrying two to seven different alleles (mean 3.70) at MHC class I and up to two alleles (mean 1.45) at MHC class II. Diversity was higher in the peptide-binding region, which suggests balancing selection. The MHC class I locus showed stronger signatures of both positive and negative selection than the MHC class II locus. Most alleles were present in more than one population. If present, private alleles generally occurred at very low frequencies in each population, except for the private alleles of MHC class I in one island population (Puerto Rico, lineage tenuirostris). CONCLUSION: Snowy Plovers exhibited an intermediate level of diversity at the MHC, similar to that reported in other Charadriiformes. The differences found in the patterns of selection between the class I and II loci are consistent with the hypothesis that different mechanisms shape the sequence evolution of MHC class I and class II genes. The rarity of private alleles across populations is consistent with high natal and breeding dispersal and the low genetic structure previously observed at neutral genetic markers in this species.

Age-dependent changes in infidelity in Seychelles warblers.

Extra-pair paternity (EPP) is often linked to male age in socially monogamous vertebrates; that is, older males are more likely to gain EPP and less likely to be cuckolded. However, whether this occurs because males improve at gaining paternity as they grow older, or because "higher quality" males that live longer are preferred by females, has rarely been tested, despite being central to our understanding of the evolutionary drivers of female infidelity. Moreover, how extra-pair reproduction changes with age within females has received even less attention. Using 18 years of longitudinal data from an individually marked population of Seychelles warblers (Acrocephalus sechellensis), we found considerable within-individual changes in extra-pair reproduction in both sexes: an early-life increase and a late-life decline. Furthermore, males were cuckolded less as they aged. Our results indicate that in this species age-related patterns of extra-pair reproduction are determined by within-individual changes with age, rather than differences among individuals in longevity. These results challenge the hypothesis-based on longevity reflecting intrinsic quality-that the association between male age and EPP is due to females seeking high-quality paternal genes for offspring. Importantly, EPP accounted for up to half of male reproductive success, emphasizing the male fitness benefits of this reproductive strategy. Finally, the occurrence of post-peak declines in extra-pair reproduction provides explicit evidence of senescence in infidelity in both males and females.

Repeatable social network node-based metrics across populations and contexts in a passerine.

Behavioural traits are considered animal personality traits when individuals differ consistently in their expression across time and across context. Here, we test this idea on three metrics derived from social interaction networks (strength, betweenness and closeness). Using experimental data from house sparrows in captive populations, and observational data from house sparrows in a wild population, we show that all three metrics consistently exhibit repeatability across both study populations and two methods of recording interactions. The highest repeatability values were estimated in male-only captive groups, whereas repeatabilities estimated in single-sex networks subsetted from mixed-sex groups showed no sex specificity. We also show that changes in social group composition led to a decrease in repeatability for up to six months. This work provides substantial and generalizable support for the notion that social network node-based metrics can be considered animal personalities. Our work suggests that social network traits may be heritable and thus could be selected for.

Development and optimization of a hybridization technique to type the classical class I and class II B genes of the chicken MHC.

The classical class I and class II molecules of the major histocompatibility complex (MHC) play crucial roles in immune responses to infectious pathogens and vaccines as well as being important for autoimmunity, allergy, cancer and reproduction. These classical MHC genes are the most polymorphic known, with roughly 10,000 alleles in humans. In chickens, the MHC (also known as the BF-BL region) determines decisive resistance and susceptibility to infectious pathogens, but relatively few MHC alleles and haplotypes have been described in any detail. We describe a typing protocol for classical chicken class I (BF) and class II B (BLB) genes based on a hybridization method called reference strand-mediated conformational analysis (RSCA). We optimize the various steps, validate the analysis using well-characterized chicken MHC haplotypes, apply the system to type some experimental lines and discover a new chicken class I allele. This work establishes a basis for typing the MHC genes of chickens worldwide and provides an opportunity to correlate with microsatellite and with single nucleotide polymorphism (SNP) typing for approaches involving imputation.

Male age and its association with reproductive traits in captive and wild house sparrows.

Evolutionary theory predicts that females seek extra-pair fertilizations from high-quality males. In socially monogamous bird species, it is often old males that are most successful in extra-pair fertilizations. Adaptive models of female extra-pair mate choice suggest that old males may produce offspring of higher genetic quality than young males because they have proven their survivability. However, old males are also more likely to show signs of reproductive senescence, such as reduced sperm quality. To better understand why old males account for a disproportionally large number of extra-pair offspring and what the consequences of mating with old males are, we compared several sperm traits of both captive and wild house sparrows, Passer domesticus. Sperm morphological traits and cloacal protuberance volume (a proxy for sperm load) of old and young males did not differ substantially. However, old males delivered almost three times more sperm to the female's egg than young males. We discuss the possibility of a post-copulatory advantage for old over young males and the consequences for females mated with old males.

Subordinate females in the cooperatively breeding Seychelles warbler obtain direct benefits by joining unrelated groups.

In many cooperatively breeding animals, a combination of ecological constraints and benefits of philopatry favours offspring taking a subordinate position on the natal territory instead of dispersing to breed independently. However, in many species individuals disperse to a subordinate position in a non-natal group ("subordinate between-group" dispersal), despite losing the kin-selected and nepotistic benefits of remaining in the natal group. It is unclear which social, genetic and ecological factors drive between-group dispersal. We aim to elucidate the adaptive significance of subordinate between-group dispersal by examining which factors promote such dispersal, whether subordinates gain improved ecological and social conditions by joining a non-natal group, and whether between-group dispersal results in increased lifetime reproductive success and survival. Using a long-term dataset on the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), we investigated how a suite of proximate factors (food availability, group composition, age and sex of focal individuals, population density) promote subordinate between-group dispersal by comparing such dispersers with subordinates that dispersed to a dominant position or became floaters. We then analysed whether subordinates that moved to a dominant or non-natal subordinate position, or became floaters, gained improved conditions relative to the natal territory and compared fitness components between the three dispersal strategies. We show that individuals that joined another group as non-natal subordinates were mainly female and that, similar to floating, between-group dispersal was associated with social and demographic factors that constrained dispersal to an independent breeding position. Between-group dispersal was not driven by improved ecological or social conditions in the new territory and did not result in higher survival. Instead, between-group dispersing females often became cobreeders, obtaining maternity in the new territory, and were likely to inherit the territory in the future, leading to higher lifetime reproductive success compared to females that floated. Males never reproduced as subordinates, which may be one explanation why subordinate between-group dispersal by males is rare. Our results suggest that subordinate between-group dispersal is used by females to obtain reproductive benefits when options to disperse to an independent breeding position are limited. This provides important insight into the additional strategies that individuals can use to obtain reproductive benefits.

Spatio-temporal variation in lifelong telomere dynamics in a long-term ecological study.

Understanding individual-level variation in response to the environment is fundamental to understanding life-history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations. Here, we study spatio-temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long-term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio-temporal variation in the social and ecological environment. We found that telomere length decreases with cross-sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross-sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error. Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island-wide insect abundance-a key resource for the insectivorous Seychelles warbler-suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex-specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth. Our long-term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long-term ecological and genetic data from multiple populations and species.

Inbreeding intensifies sex- and age-dependent disease in a wild mammal.

The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.

Reduced fitness in progeny from old parents in a natural population.

A nongenetic, transgenerational effect of parental age on offspring fitness has been described in many taxa in the laboratory. Such a transgenerational fitness effect will have important influences on population dynamics, population age structure, and the evolution of aging and lifespan. However, effects of parental age on offspring lifetime fitness have never been demonstrated in a natural population. We show that parental age has sex-specific negative effects on lifetime fitness, using data from a pedigreed insular population of wild house sparrows. Birds whose parents were older produced fewer recruits annually than birds with younger parents, and the reduced number of recruits translated into a lifetime fitness difference. Using a long-term cross-fostering experiment, we demonstrate that this parental age effect is unlikely to be the result of changes in the environment but that it potentially is epigenetically inherited. Our study reveals the hidden consequences of late-life reproduction that persist into the next generation.

Blood transcriptomes and de novo identification of candidate loci for mating success in lekking great snipe (Gallinago media).

We assembled the great snipe blood transcriptome using data from fourteen lekking males, in order to de novo identify candidate genes related to sexual selection, and determined the expression profiles in relation to mating success. The three most highly transcribed genes were encoding different haemoglobin subunits. All tended to be overexpressed in males with high mating success. We also called single nucleotide polymorphisms (SNPs) from the transcriptome data and found considerable genetic variation for many genes expressed during lekking. Among these, we identified 14 polymorphic candidate SNPs that had a significant genotypic association with mating success (number of females mated with) and/or mating status (mated or not). Four of the candidate SNPs were found in HBAA (encoding the haemoglobin α-chain). Heterozygotes for one of these and one SNP in the gene PABPC1 appeared to enjoy higher mating success compared to males homozygous for either of the alleles. In a larger data set of individuals, we genotyped 38 of the identified SNPs but found low support for consistent selection as only one of the zygosities of previously identified candidate SNPs and none of their genotypes were associated with mating status. However, candidate SNPs generally showed lower levels of spatial genetic structure compared to noncandidate markers. We also scored the prevalence of avian malaria in a subsample of birds. Males infected with avian malaria parasites had lower mating success in the year of sampling than noninfected males. Parasite infection and its interaction with specific genes may thus affect performance on the lek.

Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis.

Where wildlife disease requires management, culling is frequently considered but not always effective. In the British Isles, control of cattle tuberculosis (TB) is hindered by infection in wild badger (Meles meles) populations. Large-scale badger culling can reduce the incidence of confirmed cattle TB, but these benefits are undermined by culling-induced changes in badger behavior (termed perturbation), which can increase transmission among badgers and from badgers to cattle. Test-vaccinate/remove (TVR) is a novel approach that entails testing individual badgers for infection, vaccinating test-negative animals, and killing test-positive animals. Imperfect capture success, diagnostic sensitivity, and vaccine effectiveness mean that TVR would be expected to leave some infected and some susceptible badgers in the population. Existing simulation models predict that TVR could reduce cattle TB if such small-scale culling causes no perturbation, but could increase cattle TB if considerable perturbation occurs. Using data from a long-term study, we show that past small-scale culling was significantly associated with four metrics of perturbation in badgers: expanded ranging, more frequent immigration, lower genetic relatedness, and elevated prevalence of Mycobacterium bovis, the causative agent of TB. Though we could not reject the hypothesis that culling up to three badgers per social group might avoid perturbation, we also could not reject the hypothesis that killing a single badger prompted detectable perturbation. When considered alongside existing model predictions, our findings suggest that implementation of TVR, scheduled for 2014, risks exacerbating the TB problem rather than controlling it. Ongoing illegal badger culling is likewise expected to increase cattle TB risks.

Predictably Philandering Females Prompt Poor Paternal Provisioning.

One predicted cost of female infidelity in socially monogamous species is that cuckolded males should provide less parental care. This relationship is robust across species, but evidence is ambiguous within species. We do not know whether individual males reduce their care when paired with cheating females compared with when paired with faithful females (within-male adjustment) or, alternatively, if the males that pair with cheating females are the same males that provide less parental care in general (between-male effect). Our exceptionally extensive long-term data set of repeated observations of a wild passerine allows us to disentangle paternal care adjustment within males-within pairs and between males-while accounting for environmental variables. We found a within-male adjustment of paternal provisioning, but not incubation effort, relative to the cuckoldry in their nest. This effect was mainly driven by females differing consistently in their fidelity. There was no evidence that this within-male adjustment also took place across broods with the same female, and we found no between-male effect. Interestingly, males that gained more extrapair paternity provided less care. Data from a cross-foster experiment suggested that males did not use kin recognition to assess paternity. Our results provide insight into the role of individual variation in parental care and mating systems.