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Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

ABSTRACT: Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits (Aegithalos caudatus), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate-choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and nonkin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help toward kin.

SUBMITTER: Leedale AE

PROVIDER: S-EPMC7355050 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

Leedale Amy E AE Simeoni Michelle M Sharp Stuart P SP Green Jonathan P JP Slate Jon J Lachlan Robert F RF Robinson Elva J H EJH Hatchwell Ben J BJ

Proceedings of the National Academy of Sciences of the United States of America 20200622 27

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits (<i>Aegithalos caudatus</i>), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discriminatio ...[more]

PMID: 32571952

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Project description:AbstractWhy 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 statementTrue 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.

Project description:1. Cooperatively breeding species are typically long lived and hence, according to theory, are expected to maximize their lifetime reproductive success through maximizing survival. Under these circumstances, the presence of helpers could be used to lighten the effort of current reproduction for parents to achieve higher survival. 2. In addition, individuals of different sexes and ages may follow different strategies, but whether male and female breeders and individuals of different ages benefit differently from the presence of helpers has often been overlooked. Moreover, only one study that investigated the relationship between parental survival and the presence of helpers used capture-mark-recapture analyses (CMR). These methods are important since they allow us to account for the non-detection of individuals that are alive in the population but not detected, and thus, the effects on survival and recapture probability to be disentangled. 3. Here, we used multi-event CMR methods to investigate whether the number of helpers was associated with an increase in survival probability for male and female breeders of different ages in the sociable weaver Philetairus socius. In this species, both sexes reduce their feeding rate in the presence of helpers. We therefore predicted that the presence of helpers should increase the breeders' survival in both sexes, especially early in life when individuals potentially have more future breeding opportunities. In addition, sociable weaver females reduce their investment in eggs in the presence of helpers, so we predicted a stronger effect of helpers on female than male survival. 4. As expected we found that females had a higher survival probability when breeding with more helpers. Unexpectedly, however, male survival probability decreased with increasing number of helpers. This antagonistic effect diminished as the breeders grew older. 5. These results illustrate the complexity of fitness costs and benefits underlying cooperative behaviours and how these may vary with the individuals' sex and age. They also highlight the need for further studies on the sex-specific effects of helpers on survival.

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Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

Publications

Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

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