Explaining variation in individual fitness is a key goal in evolutionary biology. Recently, telomeres, repeating DNA sequences capping the ends of chromosomes, have gained attention as a biomarker for body state, individual quality, and ageing. However, existing research has provided mixed evidence for whether telomere length correlates with fitness components, including survival and reproductive output. Moreover, few studies have examined how telomere shortening correlates with fitness in wild populations. Here, we intensively monitored an insular population of house sparrows on Lundy Island, UK, and collected longitudinal telomere and life history data spanning 16 years from 1,225 individuals. We tested whether telomere length and/or shortening predict fitness measures, namely survival, lifespan, as well as annual and lifetime reproductive success. Telomere length positively predicted immediate survival up to one year after measurement, 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 effect of telomere length on survival translated to reproductive benefits, as birds with longer telomeres produced more genetic recruits over their lifetime, but not annually, suggesting variation in individual quality. The rate of telomere shortening, however, correlated with neither lifespan nor lifetime reproductive success. Our results provided further evidence that telomere length correlates with fitness, and they contributed to our understanding of how telomere dynamics link with individual quality.

In socially monogamous species, sexual selection not only depends on initial mate choice but also mate switching. To date, studies lack assessment of differences between passive (widowhood) and active (divorce) mate switching, longer-term fitness consequences, and how age masks reproductive costs and benefits of divorce. We investigated causes and long-term consequences of divorce and their age-dependence using longitudinal data on Seychelles warblers (Acrocephalus sechellensis), and experimentally test for short-term effects of mate-switching. Young and old males, but not females, divorced most frequently. Divorce propensity declined with pair bond duration and reproductive success in both sexes, but mate switching did not result in short-term costs. Divorcees did not gain short- or long-term fitness benefits compared to non-divorcees. In fact, female early-life divorcees that lost their breeding position had lower survival than females that never divorced. Divorce is likely a strategy to escape poor-quality partnerships, but not all divorcees benefit from divorcing.

The question of why socially monogamous females engage in extra-pair behaviour is long-standing in evolutionary biology. Recent theoretical work has moved away from the indirect-benefits hypothesis to explain female extra-pair behaviours, instead favouring suggestions that they are the result of pleiotropic effects. That is, a trait under strong positive selection in either or both sexes are genetically linked to another, often unrelated, trait. For example, where genes beneficial to female fecundity (contributing to within-pair solicitation of her social partner) are linked with extra-pair behaviour (soliciting copulations from extra-pair males). Here, we test two predictions from this hypothesis: We test the prediction that female divorce, measured from the number of social mates within a given year, is linked with (1) the number of extra-pair males and (2) the proportion of her offspring that are extra-pair. Our results suggest that females who frequently divorce social partners are more likely to produce extra-pair offspring than those who maintain social monogamy. However, by contrast, those females do not also have a higher proportion of extra-pair offspring. The number of broods initiated was also positively correlated with extra-pair males, probably through increased opportunity for extra-pair males to sire offspring over a longer breeding season. Our results provide an empirical example of a behavioural trait, beneficial to female fecundity, that is linked with extra-pair behaviour. These empirical results support the intrasexual pleiotropy hypothesis as a driver of female extra-pair behaviour.

A species’ demographic history provides important context to contemporary population genetics and a possible insight into past responses to climate change. An individual’s genome provides a window into the evolutionary history of contemporary populations. Pairwise Sequentially Markovian Coalescent (PSMC) analysis uses information from a single genome to derive fluctuations in effective population size change over the last ~5 million years. Here we apply PSMC analysis to two European nightjar (Caprimulgus europaeus) genomes, sampled in Northwest and Southern Europe, with the aim of revealing the demographic history of nightjar in Europe. We successfully reconstructed effective population size over the last 5 million years for two contemporary nightjar populations. Our analysis shows that nightjar are responsive to global climate change, with effective population size broadly increasing under stable warm periods and decreasing during cooler spans and prolonged glacial periods. PSMC analysis on the pseudo-diploid combination of the two genomes revealed fluctuations in gene flow between the populations over time, with gene flow ceasing by the last-glacial maximum. This pattern of differentiation is in line with the species utilising different refugia during glacial maxima. We suggest that nightjar in Europe may show latitudinal (East-West) genetic structuring as a result of reduced gene flow between different glacial refugia. Finally, our results suggest that migratory behaviour in nightjar likely evolved prior to the last-glacial maximum, with long-distance migration seemingly persisting throughout the Pleistocene. However, further genetic structure analysis of nightjar from known breeding sites across the species’ contemporary range is needed to fully understand the extent and origins of range-wide differentiation in the species.

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.

Understanding where and how genetic variation is maintained 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. 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, contained 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, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warblers. 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 in the populations over an extended period of time.