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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 the lifetime. This study challenges how we think of telomeres as a marker of biological age.

Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex- and environment-specific effects. Further, longitudinal parental age effects may be masked by population-level processes such as the selective disappearance of poor-quality individuals. Here, we used multigenerational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring life span and lifetime reproductive success. We found negative effects of maternal age on female offspring life span and lifetime reproductive success, which were driven by within-mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success were driven by effects on offspring life span. In contrast, there was no association between paternal age and female offspring life span or either maternal or paternal age and male offspring life span. Lifetime reproductive success, but not annual reproductive success, of male offspring increased with maternal age, but this was driven by between-mother effects. No paternal age effects were found on female offspring lifetime reproductive success but there was a positive between-father effect on male offspring lifetime reproductive success. We did not find strong evidence for environment-dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex dependent. These results add to the growing literature indicating the importance of intergenerational effects on long-term offspring performance and highlight that these effects can be an important driver of variation in longevity and fitness in the wild.

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.

Food availability modulates survival, reproduction and thereby population size. In addition to direct effects, food availability has indirect effects through density of conspecifics and predators. We tested the prediction that food availability in isolation affects reproductive success by experimentally manipulating food availability continuously for 3 years in zebra finches (Taeniopygia guttata) housed in outdoor aviaries. To this end, we applied a technique that mimics natural variation in food availability: increasing the effort required per food reward without affecting diet. Lower food availability resulted in a slight delay of start of laying and fewer clutches per season, but did not affect clutch size or number of offspring reared per annum. However, increasing foraging costs substantially reduced offspring growth. Thus, food availability in isolation did not impact the quantity of offspring reared, at the expense of offspring quality. Growth declined strongly with brood size, and we interpret the lack of response with respect to offspring number as an adaptation to environments with low predictability, at the time of egg laying, of food availability during the period of peak food demand, typically weeks later. Manipulated natal brood size of the parents did not affect reproductive success. Individuals that were more successful reproducers were more likely to survive to the next breeding season, as frequently found in natural populations. We conclude that the causal mechanisms underlying associations between food availability and reproductive success in natural conditions may be more complex than usually assumed. Experiments in semi-natural meso-populations can contribute to further unravelling these mechanisms.

Even in well-studied organisms, it is often challenging to uncover the social and environmental determinants of fitness. Typically, fitness is determined by a variety of factors that act in concert, thus forming complex networks of causal relationships. Moreover, even strong correlations between social and environmental conditions and fitness components may not be indicative of direct causal links, as the measured variables may be driven by unmeasured (or unmeasurable) causal factors. Standard statistical approaches, like multiple regression analyses, are not suited for disentangling such complex causal relationships. Here, we apply structural equation modeling (SEM), a technique that is specifically designed to reveal causal relationships between variables, and which also allows to include hypothetical causal factors. Therefore, SEM seems ideally suited for comparing alternative hypotheses on how fitness differences arise from differences in social and environmental factors. We apply SEM to a rich data set collected in a long-term study on the Seychelles warbler (Acrocephalus sechellensis), a bird species with facultatively cooperative breeding and a high rate of extra-group paternity. Our analysis reveals that the presence of helpers has a positive effect on the reproductive output of both female and male breeders. In contrast, per capita food availability does not affect reproductive output. Our analysis does not confirm earlier suggestions on other species that the presence of helpers has a negative effect on the reproductive output of male breeders. As such, both female and male breeders should tolerate helpers in their territories, irrespective of food availability.

1. The social environment in which individuals live affects their fitness and in turn population dynamics as a whole. Birds with facultative cooperative breeding can live in social groups with dominants, subordinate helpers that assist with the breeding of others, and subordinate non-helpers. Helping behaviour benefits dominants through increased reproductive rates and reduced extrinsic mortality, such that cooperative breeding might have evolved in response to unpredictable, harsh conditions affecting reproduction and/or survival of the dominants. Additionally, there may be different costs and benefits to both helpers and non-helpers, depending on the time-scale. For example, early-life costs might be compensated by later-life benefits. These differential effects are rarely analysed in the same study. 2. We examined whether helping behaviour affects population persistence in a stochastic environment and whether there are direct fitness consequences of different life-history tactics adopted by helpers and non-helpers. 3. We parameterised a matrix population model describing the population dynamics of female Seychelles warblers Acrocephalus sechellensis, birds that display facultative cooperative breeding. The stochastic density-dependent model is defined by a (st)age structure that includes life-history differences between helpers and non-helpers and thus can estimate the demographic mechanisms of direct benefits of helping behaviour. 4. We found that population dynamics are strongly influenced by stochastic variation in the reproductive rates of the dominants, that helping behaviour promotes population persistence and that there are only early-life differences in the direct fitness of helpers and non-helpers. 5. Through a matrix population model, we captured multiple demographic rates simultaneously and analysed their relative importance in determining population dynamics of these cooperative breeders. Disentangling early-life versus lifetime effects of individual tactics sheds new light on the costs and benefits of helping behaviour. For example, the finding that helpers and non-helpers have similar lifetime reproductive outputs and that differences in reproductive values between the two life-history tactics arise only in early life suggests that overall, helpers and non-helpers have a similar balance of costs and benefits when analysing direct benefits. We recommend analysing the consequence of different life-history tactics, during both early life and over the lifetime, as analyses of these different time frames may produce conflicting results.

Background Considerable research has focussed on the importance of bacterial communities within the vertebrate gut microbiome (GM). However, studies investigating the significance of other microbial kingdoms, such as fungi, are notably lacking, despite their potential to influence host processes. Here, we characterise the fungal GM of individuals living in a natural population of Seychelles warblers (Acrocephalus sechellensis). We evaluate the extent to which fungal GM structure is shaped by environment and host factors, including genome-wide heterozygosity and variation at key immune genes (major histocompatibility complex (MHC) and Toll-like receptor (TLR)). Importantly, we also explore the relationship between fungal GM differences and subsequent host survival. To our knowledge, this is the first time that the genetic drivers and fitness consequences of fungal GM variation have been characterised for a wild vertebrate population. Results Environmental factors, including season and territory quality, explain the largest proportion of variance in the fungal GM. In contrast, neither host age, sex, genome-wide heterozygosity, nor TLR3 genotype was associated with fungal GM differences in Seychelles warblers. However, the presence of four MHC-I alleles and one MHC-II allele was associated with changes in fungal GM alpha diversity. Changes in fungal richness ranged from between 1 and 10 sequencing variants lost or gained; in some cases, this accounted for 20% of the fungal variants carried by an individual. In addition to this, overall MHC-I allelic diversity was associated with small, but potentially important, changes in fungal GM composition. This is evidenced by the fact that fungal GM composition differed between individuals that survived or died within 7 months of being sampled. Conclusions Our results suggest that environmental factors play a primary role in shaping the fungal GM, but that components of the host immune system—specifically the MHC—may also contribute to the variation in fungal communities across individuals within wild populations. Furthermore, variation in the fungal GM can be associated with differential survival in the wild. Further work is needed to establish the causality of such relationships and, thus, the extent to which components of the GM may impact host evolution.

BackgroundThe gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host’s traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host’s GM. Despite this—and the documented importance of both GM and MHC variation to individual fitness—few studies have investigated the association between the GM and MHC in the wild.ResultsWe characterised MHC class I (MHC-I), MHC class II (MHC-II) and GM variation in individuals within a natural population of the Seychelles warbler (Acrocephalus sechellensis). We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). There were no associations between GM diversity andTLR3genotype, but GM diversity was positively correlated with genome-wide heterozygosity and varied with host age and field period.ConclusionsThese results suggest that components of the host’s immune system play a role in shaping the GM of wild animals. Host genotype—specifically MHC-I and to a lesser degree MHC-II variation—can modulate the GM, although whether this occurs directly, or indirectly through effects on host health, is unclear. Importantly, if immune genes can regulate host health through modulation of the microbiome, then it is plausible that the microbiome could also influence selection on immune genes. As such, host–microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations.

Behavioural patterns often differ consistently across individuals and are linked to fitness. In species with biparental care, the defence behaviour of both parents can affect reproductive success through offspring survival. In addition to the intensity of defence behaviour by both pair members, the similarity in this behaviour among parents may affect offspring survival. However, few studies have investigated the relative impact of both the intensity and similarity of defence behaviour. Here, we examined nest defence behaviour of males and females during the incubation stage in an Arctic population of barnacle geese Branta leucopsis. We calculated the repeatability of defence behaviour to test whether this behaviour is consistent within individuals and investigated how it is associated with age. In addition, we investigated how daily survival rate (DSR) of the nests until hatching is associated with nest defence behaviour and age of the parents, as well as the effect of parent similarity in nest defence behaviour as an emergent trait of the pair bond. Both male and female defence behaviour were highly repeatable. The ages of both partners within breeding pairs were positively related, but age was only significantly associated with defence behaviour in females. Further, we found high similarity in defence behaviour within breeding pairs, but the similarity and intensity of defence behaviour within breeding pairs did not predict DSR. Finally, male defence behaviour positively predicted DSR, but female defence behaviour and male and female age did not. Our results suggest that nest protection is adaptive in males but behavioural similarity of pair members does not enhance nest survival, indicating behavioural similarity itself is not adaptive but rather a by-product of different effects.

The pace-of-life syndrome (POLS) hypothesis posits that consistent between-individual variation in behavioural traits (‘animal personalities’) facilitate trade-offs in life history. Individuals who display risk averse behaviours are expected to follow a ‘slow’ pace-of-life, including short lifespan and delayed reproduction, compared to their risk-taking, ‘fast’, counterparts. Despite a breadth of empirical research testing the POLS hypothesis, findings are equivocal. This is likely due to core assumptions of the POLS hypothesis not being met, including clear trade-offs in life history, resource limited conditions, and evidence for a functional role of the behavioural trait being investigated. Here, we use long-term data from a closed island population of individually-marked Seychelles warblers to determine the relationship between repeatable exploration–avoidance personalities and an individual’s age at first breeding, lifespan and lifetime reproductive success, separately in males and females. In this population, there is a clear trade-off in reproduction and survival: individuals with a higher age at first breeding display delayed survival senescence. Further, high intraspecific competition for breeding vacancies, as well as a functional role of exploratory traits in accessing these vacancies, also exist. Using multivariate models, we found no evidence for covariation between exploratory and life history traits in either sex. We thus found no support for the POLS hypothesis, despite accounting for core components that may have masked the prevalence of POLS. Our results demonstrate that whilst particular behavioural traits may play functional roles in certain aspects of life history, they may not necessarily be influential enough to have overarching effects on an individual’s pace-of-life.

The environment experienced during development, and its impact on intrinsic condition, can have lasting outcomes for individual phenotypes and could contribute to variation in adult senescence trajectories. However, the nature of this relationship in wild populations remains uncertain, owing to the difficulties in summarizing natal conditions and in long-term monitoring of individuals from free-roaming long-lived species. Utilizing a closely monitored, closed population of Seychelles warblers (Acrocephalus sechellensis), we determine whether juvenile body mass is associated with natal socioenvironmental factors, specific genetic traits linked to fitness in this system, survival to adulthood, and senescence-related traits. Juveniles born in seasons with higher food availability and into smaller natal groups (i.e., fewer competitors) were heavier. In contrast, there were no associations between juvenile body mass and genetic traits. Furthermore, size-corrected mass—but not separate measures of natal food availability, group size, or genetic traits—was positively associated with survival to adulthood, suggesting juvenile body mass is indicative of natal condition. Heavier juveniles had greater body mass and had higher rates of annual survival as adults, independent of age. In contrast, there was no association between juvenile mass and adult telomere length attrition (a measure of somatic stress) nor annual reproduction. These results indicate that juvenile body mass, while not associated with senescence trajectories, can influence the likelihood of surviving to old age, potentially due to silver-spoon effects. This study shows that measures of intrinsic condition in juveniles can provide important insights into the long-term fitness of individuals in wild populations.

Within host populations, individuals can vary in their susceptibility to infections and in the severity and progression of disease once infected. Though mediated through differences in behaviour, resistance or tolerance, variation in disease outcomes ultimately stems from genetic and environmental (including social) factors. Despite obvious implications for the evolutionary, ecological and epidemiological dynamics of disease traits, the relative importance of these factors has rarely been quantified in naturally infected wild animal hosts. Here, we use a long-term capture-mark-recapture study of group-living European badgers (Meles meles) to characterise genetic and environmental sources of variation in host infection status by Mycobacterium bovis, the causative agent of bovine tuberculosis (bTB). We find that genetic factors contribute to M. bovis infection status, whether measured over a lifetime or across repeated captures. In the latter case the heritability (h2 ) of infection status is close to zero in cubs and yearlings but increases in adulthood. Overall, environmental influences arising from a combination of social group membership (defined in time and space) and maternal effects appear to be more important than genetic factors. Thus, while genes do contribute to among-individual variation, they play a comparatively minor role, meaning that rapid evolution of host defences under parasite-mediated selection is unlikely (especially if selection is on young animals where h2 is lowest). Conversely, our results lend further support to the view that social and early-life environments are important drivers of the dynamics of bTB infection in badger populations specifically, and of disease traits in wild hosts more generally.

Environmental conditions experienced during early life may have long-lasting effects on later-life phenotypes and fitness. Individuals experiencing poor early-life conditions may suffer subsequent fitness constraints. Alternatively, individuals may use a strategic “Predictive Adaptive Response” (PAR), whereby they respond—in terms of physiology or life-history strategy—to the conditions experienced in early life to maximize later-life fitness. Particularly, the Future Lifespan Expectation (FLE) PAR hypothesis predicts that when poor early-life conditions negatively impact an individual's physiological state, it will accelerate its reproductive schedule to maximize fitness during its shorter predicted life span. We aimed to measure the impact of early-life conditions and resulting fitness across individual lifetimes to test predictions of the FLE hypothesis in a wild, long-lived model species. Using a long-term individual-based dataset, we investigated how early-life conditions are linked with subsequent fitness in an isolated population of the Seychelles warbler Acrocephalus sechellensis. How individuals experience early-life environmental conditions may vary greatly, so we also tested whether telomere length—shorter telomers are a biomarker of an individual's exposure to stress—can provide an effective measure of the individual-specific impact of early-life conditions. Specifically, under the FLE hypothesis, we would expect shorter telomeres to be associated with accelerated reproduction. Contrary to expectations, shorter juvenile telomere length was not associated with poor early-life conditions, but instead with better conditions, probably as a result of faster juvenile growth. Furthermore, neither juvenile telomere length, nor other measures of early-life conditions, were associated with age of first reproduction or the number of offspring produced during early life in either sex. We found no support for the FLE hypothesis. However, for males, poor early-life body condition was associated with lower first-year survival and reduced longevity, indicating that poor early-life conditions pose subsequent fitness constraints. Our results also showed that using juvenile telomere length as a measure of early-life conditions requires caution, as it is likely to not only reflect environmental stress but also other processes such as growth.

Fitness is at the core of evolutionary theory, but it is difficult to measure accurately. One way to measure long-term fitness is by calculating the individual’s reproductive value, which represents the expected number of allele copies an individual passes on to distant future generations. However, this metric of fitness is scarcely used because the estimation of individual’s reproductive value requires long-term pedigree data, which is rarely available in wild populations where following individuals from birth to death is often impossible. Wild study systems therefore use short-term fitness metrics as proxies, such as the number of offspring produced. This study obtained three frequently used short-term proxies for fitness obtained at different offspring life stages (eggs, hatchlings, fledglings and recruits), and compared their ability to predict reproductive values derived from the genetic pedigree of a wild passerine bird population. We used twenty years of precise field observations and a near-complete genetic pedigree to calculate reproductive success, individual growth rate and de-lifed fitness as lifetime fitness measures, and as annual de-lifed fitness. We compared the power of these metrics to predict reproductive values and lineage survival to the end of the study period. The three short-term fitness proxies predict the reproductive values and lineage survival only when measured at the recruit stage. There were no significant differences between the different fitness proxies at the same offspring stages in predicting the reproductive values and lineage survival. Annual fitness at one year old predicted reproductive values equally well as lifetime de-lifed fitness. However, none of the short-term fitness proxies was strongly associated with the reproductive values. In summary, the commonly short-term fitness proxies capture long-term fitness with intermediate accuracy at best, if measured at recruitment stage. As lifetime fitness measured at recruit stage and annual fitness in the first year of life were the best proxies of long-term fitness, we encourage their future use.

Background The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition, and survival using data from the long-term study of a discrete natural population of the Seychelles warbler (Acrocephalus sechellensis) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons. Results We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (5% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between adult birds that survived, versus those that had died by the following breeding season. Individuals that died carried increased abundances of taxa that are known to be opportunistic pathogens, including several ASVs in the genus Mycobacterium. However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition. Conclusions These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild. However, further research is needed to establish whether changes in bacterial abundance contribute to, or are only correlated with, differential survival; this will add to our understanding of the importance of the GM in the evolution of host species living in natural populations.

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers ( Melanerpes formicivorus ), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

'The egg' illustrates the life of a bird from just before it hatches from its egg, following it as it grows up. Narrated by the focal bird in the egg, we see how the bird's sister fights off a predatory lizard to save it, and how the bird learns to fly and feed itself. The bird is a Seychelles warbler that was once critically endangered, with only 26 birds remaining in the world. Thanks to conservation efforts by scientists and Nature Seychelles, a non-government organisation, the Seychelles warblers are now living on five islands in the Seychelles and are safe from extinction. 'The egg' introduces the conservation success story behind the Seychelles warbler, and teaches children about the bird biology, including how these birds cooperate to help raise their siblings. All royalties are donated to Nature Seychelles to support their conservation work.

In cooperatively breeding species, sexually mature individuals often delay dispersal and become non-reproductive subordinates that help raise offspring. To understand how cooperative breeding can evolve, it is crucial understand the mechanisms driving delayed dispersal. Adult sex ratio (ASR) variation is often hypothesized to be an important evolutionary driver, although there is a lack of empirical evidence. Using a long-term dataset on the cooperatively breeding Seychelles warbler, we show that male juveniles are more likely to disperse when population ASR is female-biased. However, population ASR did not affect dispersal in female juveniles, indicating underlying mechanisms driving dispersal differ between the sexes.

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. 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 three years of life (both between and within individuals), with shorter telomere lengths from spring to winter and longer telomere lengths over the winter torpor period. In terms of weather conditions, linked to food availability and foraging success, cubs born in warmer, wetter springs with low rainfall variability had longer early-life (

Understanding trade‐offs in wild populations is difficult, but important if we are to understand the evolution of life histories and the impact of ecological variables upon them. Markers that reflect physiological state and predict future survival would be of considerable benefit to unraveling such trade‐offs and could provide insight into individual variation in senescence. However, currently used markers often yield inconsistent results. One underutilized measure is hematocrit, the proportion of blood comprising erythrocytes, which relates to the blood's oxygen‐carrying capacity and viscosity, and to individual endurance. Hematocrit has been shown to decline with age in cross‐sectional studies (which may be confounded by selective appearance/disappearance). However, few studies have tested whether hematocrit declines within individuals or whether low hematocrit impacts survival in wild taxa. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we demonstrated that hematocrit increases with age in young individuals (, Using long‐term data we investigated the association between haematocrit, longitudinal age and survival in a wild vertebrate population—the Seychelles warbler (Acrocephalus sechellensis). Haematocrit exhibited a distinctive age‐dependent pattern within‐individuals, and young individuals with high haematocrit had poorer survival prospects. This study highlights a novel physiological change with age that is indicative of individual condition in wild populations.

This thesis investigates the interplay of social evolution and population dynamics in Seychelles warblers, passerine birds with facultative cooperative breeding where some breeders receive help from other individuals when raising offspring. The thesis aims to elucidate how individual fitness is determined by the combination of individual traits and life-history events with its social and non-social environment and how fitness variation may result in complex eco-evolutionary dynamics. To this end, by combining advanced statistical methods with data-driven simulations, I analyzed field data collected between 1995 and 2019 on the life-history and demography of Seychelles warblers inhabiting Cousin Island in the Republic of Seychelles. By employing a data-driven matrix model, in Chapter 2, I show that the presence of helpers could have a stabilizing effect on the population dynamics under density dependence and environmental stochasticity. Chapter 3 evaluates the performance of structural equation modelling in inferring causal mechanisms that drive variations in individual fitness by applying an individual-based model. I show that structural equation models are useful but data-hungry. In Chapter 4, I examine the causal relationships between individual-, group- and population-level drivers of fitness in breeding females. Fitness drivers might have played an essential role in the evolution of individual differences between dominant females. Chapter 5 investigates how experience, social environment, and territory quality influenced the overall reproductive success of highly promiscuous dominant females and males.

Despite extensive evidence of senescence, the decline in performance with age, in wild populations, the drivers ofindividual variation in senescence patternsare still unresolved. In this thesis,I study how early-life environmental, genetic and transgenerational effects contribute to individual variation in senescence patterns, using telomere dynamics,ina wild population ofEuropean badgers (Meles meles).I discovered that telomere length forms a complex relationship with age,withboth decreases and increases in telomere length that cannot be fully explained by measurement error. Telomere length was not sex-specific, but early-life telomere length predicts survival to adulthood (>1 year old) and lifespan. Within-individual changes in telomere length could be due to age-related changesin leukocyte cell composition in response to social conditions. While variation in (early-life)telomere length was associatedwith the abundance and variation in food availability, andnatal but not adultsocial conditions, I found no evidence for heritability of telomere length or transgenerationaleffects, through parental age at conceptioneffects. Additionally, individuals experiencingmatching early-and later-life conditions had longer lifespans,even though there was only moderate autocorrelation in environmental quality, but this also depended on the mean environmental qualityacross adulthood. Ialsodeveloped a novel approach to the analysis of long-term studies, termed slicing, which overcomes problems with confounding effects and cross-classified data structures.My research shows that individual variation in telomere length and senescence is a consequence of early-life environmental, not genetic or transgenerational, effects in European badgers. In addition, I show the potential for adaptive responses in anticipation of the adult environment and the importance ofstudying both the mean of and variability in early-life conditions to fully understand the selective pressures on senescence.

Evidence for age-related changes in innate and adaptive immune responses is increasing in wild populations. Such changes have been linked to fitness, and knowledge of the factors driving immune response variation is important for understanding the evolution of immunity. Age-related changes in immune profiles may be owing to factors such as immune system development, sex-specific behaviour and responses to environmental conditions. Social environments may also contribute to variation in immunological responses, for example, through transmission of pathogens and stress arising from resource and mate competition. Yet, the impact of the social environment on age-related changes in immune cell profiles is currently understudied in the wild. Here, we tested the relationship between leukocyte cell composition (proportion of neutrophils and lymphocytes [innate and adaptive immunity, respectively] that were lymphocytes) and age, sex and group size in a wild population of European badgers ( Meles meles ). We found that the proportion of lymphocytes in early life was greater in males in smaller groups compared to larger groups, but with a faster age-related decline in smaller groups. By contrast, the proportion of lymphocytes in females was not significantly related to age or group size. Our results provide evidence of sex-specific age-related changes in immune cell profiles in a wild mammal, which are influenced by the social environment.

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.

Natural selection is expected to favor males that invest more in offspring they sire. We investigated the relationship between paternity and male behavior in the acorn woodpecker (Melanerpes formicivorus), a cooperative breeder that lives in family groups including offspring that remain on their natal territory, sometimes for years, and cobreeders of both sexes. Regardless of group composition, only one communal nest is attended at a time. Whereas cobreeding females share maternity equally, one male usually sires the majority of young in the group’s communal nest. Copulations are rarely observed, and thus it has not been possible to link paternity to sexual behavior. There were no differences among cobreeder males that did or did not sire young in their propensity to roost in the nest cavity at night. However, cobreeder males that attended females continuously prior to egg-laying were more likely to successfully sire young than males that did not, and the relative share of feeding visits and time spent at the subsequent nest were positively related to a male’s realized paternity. These differences in male behavior were partly due to differences among males and partly to plasticity in male behavior covarying with paternity share. Feedings by males successfully siring young also involved a larger proportion of nutritionally valuable insect prey. Males are aware of their paternity success, apparently because of their relative access to females prior to egg laying, and provide more paternal care at nests in which they are more likely to have sired young.

Why so much variation in extra-pair parentage occurs within and among populations remains unclear. Often the fitness costs and benefits of extra-pair parentage are hypothesised to explain its occurrence; therefore, linking extra-pair parentage with traits such as personality (behavioural traits that can be heritable and affect reproductive behaviour) may help our understanding. Here, we investigate whether reproductive outcomes and success are associated with exploratory behaviour in a natural population of cooperatively breeding Seychelles warblers (Acrocephalus sechellensis) on Cousin Island. Exploratory behaviour correlates positively with traits such as risk-taking behaviour and activity in other wild bird species and might promote extra-pair mating by increasing the rate at which potential extra-pair partners are encountered. We therefore predicted that fast-exploring individuals would have more extra-pair offspring. There is also a potential trade-off between pursuing extra-pair parentage and mate guarding in males. We therefore also predicted that fast-exploring males would be more likely to pursue extra-pair parentage and that this would increase the propensity of their mate to gain extra-pair parentage. We found that neither the total number of offspring nor the number of extra-pair offspring were associated with a male’s or female’s exploratory behaviour. However, there was a small but significant propensity for females to have extra-pair fertilisations in pairs that were behaviourally disassortative. Overall, we conclude that, due to the small effect size, the association between exploratory behaviour and extra-pair paternity is unlikely to be biologically relevant. Significance statement True genetic monogamy is rare, even in socially monogamous systems, and multiple factors, such as behaviour, social structure, morphology and physiology, determined by the biological system can cause variation in extra-pair parentage (EPP). Therefore, investigating the inherent differences in these factors among individuals could be informative. We investigated whether reproductive outcomes/success are associated with differences in the propensity to explore novel environments/objects in a promiscuous, island-dwelling cooperatively breeding bird, the Seychelles warbler. Our results showed that exploratory behaviour was not associated with the number of offspring produced by an individual, and thus the long-term fitness consequences of different exploratory tendencies did not differ. We also found that the propensity to engage in EPP in females was higher in dissimilar behavioural pairs, but due to the small effect size, we hesitate to conclude that there are personality-dependent mating outcomes in the population. Electronic supplementary material The online version of this article (10.1007/s00265-018-2448-z) contains supplementary material, which is available to authorized users.

Lay Summary An individual’s circumstances or properties—also known as state—maybe a mechanism encouraging behavioral differences among individuals. We investigated whether exploration was associated with social state or reproductive state (i.e., insect abundance at year of birth) in a wild cooperative breeder. We found fast novel object exploration was associated with young individuals born into years of high insect abundance (i.e., low future reproductive state), suggesting this behavior is reproductive state-dependent., Personality is an intriguing phenomenon in populations because it constrains behavioral flexibility. One theory suggests that personality could be generated and maintained if dependent on asset protection. It is predicted that trade-offs with fitness expectations and survival probability encourage consistent behavioral differences among individuals (personality). Although not mutually exclusive, the social niche specialization hypothesis suggests that a group of individuals that repeatedly interact will develop personality to avoid costly social conflict. The point at which behavioral consistency originates in the social niche hypothesis is still unclear, with predictions for development after a change in social status. In the facultative cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), residing on Cousin Island, breeding vacancies are limited and this forces individuals into different social roles. We used this system to test whether reproductive and social state predicted among-individual differences in exploration. We had 2 predictions. First, that an individual’s start in life can predict personality, whereby young individuals with a good start to life (associated with early age reproduction and earlier onset survival senescence) are fast explorers, suggesting reproductive state-dependence. Second, that an individual’s social status can predict personality, whereby dominant individuals will be fast explorers, suggesting that the behavior is social state-dependent. Neither of the behaviors was associated with social state and social state did not affect behavioral consistency. However, novel object exploration was associated with a proxy of reproductive state. Our results provide further support for state being a mechanism for generating individual differences in behavior.

IntroductionThe Seychelles warbler (Acrocephalus sechellensis), a passerine endemic to the Seychelles archipelago, is a facultatively cooperative breeder that lives either in pairs or small groups. Breeding groups normally consist of a dominant pair and one to three subordinates, although up to nine have been observed. Subordinates can be of either sex, and are often offspring that have delayed dispersal and remained in their natal territory (Komdeur 1992; Richardson et al. 2002; Eikenaar et al. 2008, 2010). By the 1960s the last remnant population of this then critically endangered species was confined to Cousin Island (Figure 12.1). Subsequent conservation actions, including the restoration of forest habitat and the establishment of new populations through translocations, have provided unique opportunities to study the evolutionary ecology of cooperative breeding in this species. We have followed the entire world population of the Seychelles warbler since our study started in 1981. In 1997, however, we increased the intensity of work on Cousin and since then nearly all individuals, including fledglings, have been captured, ringed, blood sampled, sexed, and monitored for breeding and status. Molecular tools have been used to assign the sex and genetic parentage of young birds and to determine levels of relatedness between individuals. In addition, a comprehensive set of behavioral, life history, and annual fitness parameters have been recorded for nearly all individuals, providing important opportunities for assessing changes in social behavior. The lack of interisland dispersal (Komdeur et al. 2004a), combined with sampling of the entire population, provides a rare opportunity to monitor the survival, reproduction, and lifetime fitness of all individuals within the population. Our long-term research program into cooperative breeding, hand-in-hand with conservation actions, has created an experimental system in which we can attempt to unravel the factors that alter the cost-benefit trade-offs of cooperative breeding. Over time, this system has become proof of the power of the experimental methods and of the corrective value of long-term studies, where iterative examination with longer-term data sheds new insights on short-term findings. Here we detail various findings that have allowed us to uncover how changing social and ecological factors influence the form and function of reproductive competition and cooperation in the Seychelles warbler. We also outline how molecular genetic tools have given us a better understanding of the species’ cooperative breeding system and the selective factors that favor switching between different forms of cooperative and independent breeding.

Telomere length predicts survival in birds, and many stressors that presumably reduce fitness have also been linked to telomere length. The response to selection of telomere length will be largely determined by the heritability of this trait; however, little is known about the genetic component of telomere length variation in animals other than humans. Moreover, published heritability estimates of telomere length are based on telomere measurements with techniques that do not distinguish between terminal telomeres, which are susceptible to age and stress, and the interstitial telomeric repeats, which are relatively inert. Heritability estimates that combine interstitial and terminal telomeres are difficult to interpret in species such as birds, where interstitial telomeres are often numerous. We estimated the heritability of terminal telomere length in a captive Zebra Finch population of cross-fostered (half-)siblings using data obtained with an electrophoresis technique that excludes the interstitial repeats from the measurements. We used both a Bayesian quantitative genetic 'animal' model and a frequentist sibling regression approach to estimate heritability. With the animal model, we estimated a high heritability of telomere length (h (2) = 0.99, 95 % credible interval = 0.87-1), but had insufficient statistical power to separate parental and permanent environment effects. The frequentist approach yielded similar heritability estimates, although with large confidence intervals. We used general linear mixed models to disentangle variance components of telomere length. The relative contributions of the individual, mother and father to telomere length variation were statistically indistinguishable at 23-31 %. Chicks were cross-fostered 4-days after hatching, and no effect of rearing nest was found, indicating that any undetected environmental effects exerted their influence prior to, or soon after, hatching. Thus, we conclude that telomere length resemblance between relatives is high and proportional to their relatedness, but we cannot conclusively distinguish between genetic and other forms of inheritance.

Studies of the evolution of the major histocompatibility complex (MHC) have been central to the understanding sexual selection and pathogen-mediated selection. The European badger Meles meles is well suited for exploring such questions because of its life history characteristics, reproductive biology and mating system. In this thesis, I examined both MHC class I and class II genes. Seven putatively functional sequences were found for class I genes and four for class II DRB genes. Evidence of past balancing selection of both genes was demonstrated by the dNdS ratio, by positive selection at the antigen-binding site (ABS) and by trans-species polymorphism of alleles within other mustelids and carnivores. MHC class I genes also showed evidence of concerted evolution, but domains showed different evolutionary histories. MHC genes may influence microbiota and odour of an individual and influence mating preferences. I examined the bacterial community of the subcaudal gland secretion and demonstrated a high number of bacterial species (56 operational taxonomic units), which cubs exhibited a higher diversity than adults. The microbiota may lead to an individual-specific odour as a cue signaling the MHC genotype of potential mating partners. I report the first evidence for a MHC- based mating preference in carnivores. Female badgers showed a MHC-assortative mate choice towards breeding with males that had functionally similar MHC genes, for MHC class II DRB genes. This applied to neighbouring-group matings. I also found considerable annual fluctuation in the occurrence of MHC-based mate choice. Based on genome-wide background in the same mating randomizations I found no evidence of inbreeding, which indicated that MHC similarity was apparently the actual target of mate choice. In line with MHC-assortative mate choice, MHC heterozygosity had no influence on the co-infection status. Individual MHC alleles did, however, associate with resistance and susceptibility to specific pathogens, suggesting that MHC diversity may be driven and maintained by pathogen-mediated selection through rare-allele advantages and/or fluctuating selection. My study of genetic characteristics, mate choice and pathogen pressures in a wild population revealed past and contemporary evolutionary process of the MHC genes. This increases knowledge of how the MHC may affect mating behaviour and sexual selection, ultimately influencing population processes.

The evolution of extra-group paternity (EGP) is a contentious issue in evolutionary biology. This thesis examines the factors and adaptive benefits driving EGP in a high-density, group-living population of European badgers (Meles meles). To improve power to assign parentage, I isolated and characterised 21 new polymorphic microsatellite markers. I genotyped 83% of 1410 badger trapped 1987‒2010 using 35 autosomal microsatellite markers. Maternity and paternity were assigned at 80% confidence ca. 82% of individuals. 48% of paternities were extra-group, where 85% were attributable to neighbouring-group males and EGP was detected in 47% of litters; thus badger social group do not correspond with a breeding unit. I tested whether indirect genetic benefits explain these high EGP rates. (1) ‘Good-gene-as-heterozygosity Hypothesis’: Paternal heterozygosity, but not maternal or an individual’s own heterozygosity, associated positively with first-year survival probability. Under benign environmental conditions, cubs fathered by more heterozygous males had a higher first year survival probability. Despite this correlation, the EGP rate per litter correlated with neither average nor maximum within-group heterozygosity of candidate fathers. (2) Fitness benefit Hypothesis: Extra-group offspring (EGO) had lower first-year survival probability and lived 1.3 years less than within-group offspring (WGO). Female WGO produced more litters and offspring over their lifetime than female EGO, whereas male EGO produced more offspring than male WGO. (3) Inbreeding avoidance hypothesis: The EGP rate within a litter increased with greater average pair-wise relatedness between mothers and within-group candidate fathers. No inbreeding depression on first-year survival probability was detected, but small sample sizes limited statistical power. Socio-ecologically, at the litter level, EGP correlated negatively with the number of within-group candidate fathers, and positively with neighbouring-group candidate fathers. In conclusion, EGP in badgers may reduce inbreeding and be maintained in the population through a sex-specific antagonistic selection and indirect genetic benefits may occur when the total fitness benefits of producing extra-group sons outweigh the costs of producing extra-group daughters. These indirect genetic benefits only partially explain the evolution of promiscuity in European badgers, highlighting that evolutionary factors underlying promiscuity remain unclear.

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 (

Species are facing environmental challenges caused by rapidly changing environments induced by climate change. In tropical regions, climate change causes increasing frequencies of extreme weather,like droughts or extreme rainfall. Natural selection is usually slow and adaptations through phenotypic plasticity are limited, thus species might need more mechanisms to cope with change, like cooperative breeding. Rainfall is an important cue for onset of breeding in many tropical bird species, so young are born when food abundance is highest. We explore the effect of rainfall on the social behaviour and life history of the insectivorous Seychelles warblers (Acrocephalus sechellensis), a facultative cooperative58breeder, using long-term data. We expect that with increasing amounts of rain food resources will increase, and thus reproductive output and survival will increase. If so, in dry periods, reproductive output of breeding pairs will be limited, but cooperative breeding may counteract this negative effect because helpers assist with feeding young. We expect that in dry periods breeding pairs produce more offspring of the helping sex, who stay in their natal territory and become helpers in the following year. Rainfall positively affected insect abundance. With increasing rainfall, survival of individuals during the breeding season and reproductive output, especially for cooperatively breeding groups, increased. With more rainfall, also more daughters (the helping sex) were produced, resulting in more group formation the year after. Thus, in contrast to our expectations, Seychelles warblers form social groups in favourable conditions, indicating that group living may be costly and thus not a solution to coping with changing environments. This study showed that the interaction between the environment and life histories,including social behaviour, is complex, and important to consider when studying the impact of changing environments on species survival