Explaining variation in life expectancy between individuals of the same age is fundamental to our understanding of population ecology and life history evolution. Variation in the length and rate of ...loss of the protective telomere chromosome caps has been linked to cellular lifespan. Yet, the extent to which telomere length and dynamics predict organismal lifespan in nature is still contentious. Using longitudinal samples taken from a closed population of Acrocephalus sechellensis (Seychelles warblers) studied for over 20 years, we describe the first study into life‐long adult telomere dynamics (1–17 years) and their relationship to mortality under natural conditions (n = 204 individuals). We show that telomeres shorten with increasing age and body mass, and that shorter telomeres and greater rates of telomere shortening predicted future mortality. Our results provide the first clear and unambiguous evidence of a relationship between telomere length and mortality in the wild, and substantiate the prediction that telomere length and shortening rate can act as an indicator of biological age further to chronological age when exploring life history questions in natural conditions.
The question of why socially monogamous females engage in extra‐pair behaviour is long‐standing in evolutionary biology. Due to a lack of empirical support among passerine birds, recent work has ...moved away from the indirect‐benefits hypothesis to explain extra‐pair mating behaviour by females, instead favouring the hypothesis that this is the result of a pleiotropic effect. That is, a trait under strong positive selection in either or both sexes are genetically linked with another, potentially unrelated, trait. For example, genes beneficial to female fecundity (that promote within‐pair solicitation of mating from a male partner) might also lead to extra‐pair behaviour (by also promoting solicited copulations from extra‐pair males). Here, we test two predictions from this hypothesis: We test the prediction that female divorce, measured as the number of social mates within a given year, is linked with 1) the number of extra‐pair males engaged by the female and 2) the proportion of the female's offspring that are extra‐pair. Our results show that females who divorce their social partner are more likely to produce extra‐pair offspring than those who maintain social monogamy, supporting the pleiotropy hypothesis. However, those females did not also have a higher proportion of extra‐pair offspring. The number of broods initiated was also positively correlated with the number of extra‐pair males that sired a female's offspring, probably through increased opportunity for extra‐pair males to sire offspring over a longer breeding season. Our results support the intrasexual pleiotropy hypothesis as a driver of female extra‐pair behaviour.
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.
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.
Significance As parents age, gamete quality declines. If this decline affects the next generation, it could influence the evolution of longevity. Older parents often produce offspring of low fitness in the laboratory. Our long-term data from a natural bird population shows, for the first time to our knowledge, a transgenerational reduction in fitness of the next generation associated with parental age. We use a 10-year cross-fostering experiment to exclude environmental explanations. Our results challenge the currently favored hypothesis in evolutionary biology and behavioral ecology that old age signals high quality in mating partners. Our results imply a substantial cost of reproducing with older, rather than younger, partners. The results inform increasing concern about delayed reproduction in medicine, sociology, and conservation biology.
Fitness in birds has been shown to be negatively associated with anthropogenic noise, but the underlying mechanisms remain obscure. It is however crucial to understand the mechanisms of how urban ...noise impinges on fitness to obtain a better understanding of the role of chronic noise in urban ecology. Here, we examine three hypotheses on how noise might reduce reproductive output in passerine birds: (H1) by impairing mate choice, (H2) by reducing territory quality and (H3) by impeding chick development.
We used long-term data from an island population of house sparrows, Passer domesticus, in which we can precisely estimate fitness. We found that nests in an area affected by the noise from large generators produced fewer young, of lower body mass, and fewer recruits, even when we corrected statistically for parental genetic quality using a cross-fostering set-up, supporting H3. Also, individual females provided their young with food less often when they bred in the noisy area compared to breeding attempts by the same females elsewhere. Furthermore, we show that females reacted flexibly to increased noise levels by adjusting their provisioning rate in the short term, which suggests that noise may be a causal factor that reduces reproductive output. We rejected H1 and H2 because nestbox occupancy, parental body mass, age and reproductive investment did not differ significantly between noisy and quiet areas.
OUR RESULTS SUGGEST A PREVIOUSLY UNDESCRIBED MECHANISM TO EXPLAIN HOW ENVIRONMENTAL NOISE CAN REDUCE FITNESS IN PASSERINE BIRDS: by acoustically masking parent-offspring communication. More importantly, using a cross-fostering set-up, our results demonstrate that birds breeding in a noisy environment experience significant fitness costs. Chronic noise is omnipresent around human habitation and may produces similar fitness consequences in a wide range of urban bird species.
Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling 1–8 and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as ...astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids 9, 10. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19yb), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19yb is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability.
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•The yellowbeak mutation maps to a narrow region of chromosome 8 with a CYP cluster•CYP2J19 loci most likely encode ketolases that generate red ketocarotenoids•CYP2J19 loci are involved both in red coloration and red retinal oil droplets•Involvement of cytochrome P450s provides a novel mechanism of signal honesty
Mundy et al. have identified genes required for the bright-red coloration that many birds use for communication, such as attracting mates. They uncover a genetic connection between red coloration and color vision in birds and propose that redness may be an honest signal of mate quality by indicating a bird’s ability to detoxify harmful substances.
Traditional models for female extra‐pair matings assume that females benefit indirectly from extra‐pair mating behaviour. Under these so‐called adaptive models, extra‐pair males are hypothesized to ...have more compatible genotypes, larger body size, exaggerated ornaments or to be older than cuckolded males. Alternatively, (‘nonadaptive’) models that consider female extra‐pair matings to be a by‐product posit that female extra‐pair mating can be maintained even if there is no benefit to females. This could happen if, for example, males gained fitness benefits from extra‐pair mating, while female and male extra‐pair mating behaviours were genetically correlated. Extra‐pair males are also expected to be older and larger if this improves their ability to convince or coerce females to mate. We investigated whether a female's extra‐pair mates differed from her cuckolded mate in both genetic and phenotypic traits by analysing data from an insular house sparrow population. We found that extra‐pair males were older than cuckolded males, consistent with both models. However, in contrast to the expectations from from adaptive models, extra‐pair and cuckolded males were of similar genetic relatedness, and hence expected compatibility, with the female, and had comparable body size and secondary sexual traits. We also updated previous meta‐analyses examining differences between extra‐pair and cuckolded males. The meta‐analytic results matched results from our house sparrow case study. Although we cannot completely exclude indirect benefits for females, nonadaptive models may better explain female extra‐pair matings. These neglected alternative models deserve more research attention, and this should improve our understanding of the evolution of mating systems.
In a rapidly changing world, it is of fundamental importance to understand processes constraining or facilitating adaptation through microevolution. As different traits of an organism covary, genetic ...correlations are expected to affect evolutionary trajectories. However, only limited empirical data are available.
We investigate the extent to which multivariate constraints affect the rate of adaptation, focusing on four morphological traits often shown to harbour large amounts of genetic variance and considered to be subject to limited evolutionary constraints. Our data set includes unique long-term data for seven bird species and a total of 10 populations. We estimate population-specific matrices of genetic correlations and multivariate selection coefficients to predict evolutionary responses to selection. Using Bayesian methods that facilitate the propagation of errors in estimates, we compare (1) the rate of adaptation based on predicted response to selection when including genetic correlations with predictions from models where these genetic correlations were set to zero and (2) the multivariate evolvability in the direction of current selection to the average evolvability in random directions of the phenotypic space. We show that genetic correlations on average decrease the predicted rate of adaptation by 28%. Multivariate evolvability in the direction of current selection was systematically lower than average evolvability in random directions of space. These significant reductions in the rate of adaptation and reduced evolvability were due to a general nonalignment of selection and genetic variance, notably orthogonality of directional selection with the size axis along which most (60%) of the genetic variance is found.
These results suggest that genetic correlations can impose significant constraints on the evolution of avian morphology in wild populations. This could have important impacts on evolutionary dynamics and hence population persistence in the face of rapid environmental change.
Helping by group members is predicted to lead to delayed senescence by affecting the trade-off between current reproduction and future survival for dominant breeders. Here we investigate this ...prediction in the Seychelles warbler, Acrocephalus sechellensis, in which mainly female subordinate helpers (both co-breeders and non-breeding helpers) often help dominants raise offspring. We find that the late-life decline in survival usually observed in this species is greatly reduced in female dominants when a helper is present. Female dominants with a female helper show reduced telomere attrition, a measure that reflects biological ageing in this and other species. Finally, the probability of having female, but not male, helpers increases with dominant female age. Our results suggest that delayed senescence is a key benefit of cooperative breeding for elderly dominants and support the idea that sociality and delayed senescence are positively self-reinforcing. Such an effect may help explain why social species often have longer lifespans.
Theory predicts that individuals behave altruistically towards their relatives. Hence, some form of kin recognition is useful for individuals to optimize their behavior. In species that display ...bi-parental care and are subject to extra-pair matings, kin recognition theoretically can allow cuckolded fathers to reduce their parental investment, and thus optimize their fitness. Whether this is possible remains unclear in birds. This study investigates whether males provide differential parental care depending on relatedness, as a proxy to recognizing chicks in their nest as kin or not. We cross-fostered House sparrow (Passer domesticus) chicks after hatching, and then expected that fathers would show a decrease in their parental efforts when tending to a clutch of unrelated offspring. House sparrow males are able to adjust their parental care to the identity of their partner, making them an ideal study species. However, there was no significant effect of relatedness on provisioning rates. This suggests that sparrows may not be capable of kin recognition, or at least do not display kin discrimination despite its apparent evolutionary advantage.
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