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.

A meta-analysis on the heritability of vertebrate telomere length.

Telomere dynamics are linked with both cellular and organismal senescence, and life history, individual quality and health. Telomere dynamics, particularly telomere length, have therefore garnered much research interest in evolutionary biology. To examine the evolution of telomere length, it is important to quantify its heritability, the proportion of total variation explained by additive genetic effects. Many studies have quantified telomere length heritability, but estimates are varied, and no general conclusion has been drawn. Additionally, it is unclear whether biological and methodological factors influence telomere length heritability estimates. We present the first meta-analysis of telomere length heritability, using 104 estimates from 43 studies over 18 vertebrate species. We calculated an overall mean heritability and examined how estimates varied by study, phylogeny, species-specific ecology, environmental setting, age at sampling, laboratory methods, statistical methods, sex and repeated measurements. Overall heritability was moderate (44.9%, 95% CI: 25.2-64.7%), and there was considerable heterogeneity in heritability estimates, in particular among studies and estimates. Laboratory method influenced heritability estimates, with in-gel hybridization TRF yielding higher heritabilities than qPCR and Southern blot TRF. There was also an effect from statistical method, with twin-based and SNP-based estimates lower than correlation-based or pedigree-based estimates. Our results highlight an overall heritable basis of telomere length, and we recommend future research on a wider range of taxa, and the use of variance-partitioning methods with relatedness or SNP data over correlation methods to minimize heritability estimation bias.

Not so social in old age: demography as one driver of decreasing sociality.

Humans become more selective with whom they spend their time, and as a result, the social networks of older humans are smaller than those of younger ones. In non-human animals, processes such as competition and opportunity can result in patterns of declining sociality with age. While there is support for declining sociality with age in mammals, evidence from wild bird populations is lacking. Here, we test whether sociality declines with age in a wild, insular bird population, where we know the exact ages of individuals. Using 6 years of sociality data, we find that as birds aged, their degree and betweenness decreased. The number of same-age birds still alive also decreased with age. Our results suggest that a longitudinal change in sociality with age may be, in part, an emergent effect of natural changes in demography. This highlights the need to investigate the changing costs and benefits of sociality across a lifetime.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

Indirect genetic effects increase heritability estimates for male and female extra-pair reproduction.

The question of why females engage in extra-pair behaviors is long-standing in evolutionary biology. One suggestion is that these behaviors are maintained through pleiotropic effects on male extra-pair behaviors (genes controlling extra-pair reproduction are shared between sexes, but only beneficial to one sex, in this case, males). However, for this to evolve extra-pair reproduction must be both heritable and positively genetically correlated between sexes. Previous studies have suggested low heritability with no evidence for between-sex genetic correlations in extra-pair reproduction. However, these have not considered indirect genetic effects (derived from the behavior of others, IGEs) from the social partner, the influence of the social partner's genotype on the phenotype of an individual, despite the potential of IGEs to uncover hidden heritable variation. Using data from a closed-house sparrow population with a genetic pedigree spanning two decades, we tested the influence of social partner IGEs on heritable variation and genetic correlation estimates of extra-pair reproduction. We found that the inclusion of IGEs resulted in larger heritable genetic variance for both male and female extra-pair heritability. While IGEs did not change between-sex genetic correlations, we found they reduced uncertainty in those estimates. Future studies should consider the effect of IGEs on the mechanisms of sex-specific extra-pair reproduction.

What is the best fitness measure in wild populations? A case study on the power of short-term fitness proxies to predict reproductive value.

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 compared two frequently used short-term metrics 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 were strongly associated with the reproductive values. The commonly used short-term fitness proxies best predict long-term fitness when measured at recruitment stage. Thus, because lifetime fitness measured at recruit stage and annual fitness in the first year of life were the best proxies of long-term fitness in short-lived birds, we encourage their future use.

Individual variation in reaction norms but no directional selection in reproductive plasticity of a wild passerine population.

In the plant-insect-insectivorous bird food chain, directional changes in climate can result in mismatched phenology, potentially affecting selection pressures. Phenotypic plasticity in the timing of breeding, characterized by reaction norm slopes, can help maximize fitness when faced with earlier prey emergence. In temperate passerines, the timing of tree budburst influences food availability for chicks through caterpillar phenology and the resulting food abundance patterns. Thus, the timing of tree budburst might serve as a more direct proxy for the cue to time egg-laying. The evolutionary potential of breeding plasticity relies on heritable variation, which is based upon individual variation, yet studies on individual variation in plasticity are few. Here, we tested for the laying date-budburst date and the clutch size-laying date reaction norms, and examined 1) the among-individual variance in reaction norm intercepts and slopes; and 2) the selection differentials and gradients on these intercepts and slopes. Using long-term data of oak (genus Quercus) budburst and blue tit (Cyanistes caeruleus) reproduction, we applied within-subject centering to detect reaction norms, followed by bivariate random regression to quantify among-individual variance in reaction norm properties and their covariance with fitness. Individuals significantly differed in intercepts and slopes of both laying date-budburst date and clutch size-laying date reaction norms, and directional selection was present for an earlier laying date and a larger clutch size (intercepts), but not on plasticity (slopes). We found that individuals have their own regimes for adjusting egg-laying and clutch size. This study provides further support of individual variation of phenotypic plasticity in birds.