Kith or Kin? Familiarity as a Cue to Kinship in Social Birds

© Copyright © 2020 Leedale, Li and Hatchwell. Interacting with relatives provides opportunities for fitness benefits via kin-selected cooperation, but also creates potential costs through kin competition and inbreeding. Therefore, a mechanism for the discrimination of kin from non-kin is likely to be critical for individuals of many social species to maximize their inclusive fitness. Evidence suggests that genetic cues to kinship are rare and that learned or environmental cues offer a more parsimonious explanation for kin recognition in most contexts. This is particularly true among cooperatively breeding birds, where recognition of familiar individuals is usually regarded as the most plausible mechanism for kin discrimination. In this article, we first review the evidence that familiarity provides an effective decision rule for discrimination of kin from non-kin in social birds. We then consider some of the complexities of familiarity as a cue to kinship, especially the problems of how individuals become familiar, and how familiar individuals are recognized. We conclude that while familiarity as a mechanism for kin recognition may be more parsimonious and widespread than genetic mechanisms, its apparent simplicity as a decision rule governing social interactions may be deceptive. Finally, we identify directions for future research on familiarity as a kin recognition mechanism in social birds and other taxa

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

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

Variation in helper effort among cooperatively breeding bird species is consistent with Hamilton's Rule.

Investment by helpers in cooperative breeding systems is extremely variable among species, but this variation is currently unexplained. Inclusive fitness theory predicts that, all else being equal, cooperative investment should correlate positively with the relatedness of helpers to the recipients of their care. We test this prediction in a comparative analysis of helper investment in 36 cooperatively breeding bird species. We show that species-specific helper contributions to cooperative brood care increase as the mean relatedness between helpers and recipients increases. Helper contributions are also related to the sex ratio of helpers, but neither group size nor the proportion of nests with helpers influence helper effort. Our findings support the hypothesis that variation in helping behaviour among cooperatively breeding birds is consistent with Hamilton's rule, indicating a key role for kin selection in the evolution of cooperative investment in social birds

Neighbours' Breeding Success and the Sex Ratio of Their Offspring Affect the Mate Preferences of Female Zebra Finches

Several hypotheses on divorce predict that monogamous pairs should split up more frequently after a breeding failure. Yet, deviations from the expected pattern “success-stay, failure-leave” have been reported in several species. One possible explanation for these deviations would be that individuals do not use only their own breeding performance (i.e., private information) but also that of others (i.e., public information) to decide whether or not to divorce. To test this hypothesis, we investigated the relative importance of private and public information for mate choice decisions in female zebra finches (Taeniopygia guttata).We manipulated the reproductive performance of breeding pairs and measured females' preferences for their mate and the neighbouring male first following pair formation and then seven weeks later when all females had laid eggs and the young were independent. Although all females reduced their preference for their mate after a breeding failure, the decrease was significant only when the neighbouring pair had reproduced successfully. Furthermore, there was no evidence that females biased the sex ratio of their offspring according to their mate's attractiveness. On the other hand, after reproduction, both successful and unsuccessful females increased their preferences for males who had produced a larger proportion of sons. Despite the fact that other mechanisms may have also contributed to our findings, we suggest that females changed their mate preferences based on the proportion of sons produced by successful males, because offspring sex ratio reflects the male's testosterone level at the moment of fertilization and hence is an indicator of his immune condition

Demographic routes to variability and regulation in bird populations

There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season

Helpers and egg investment in the cooperatively breeding acorn woodpecker: testing the concealed helper effects hypothesis

In cooperatively breeding acorn woodpeckers (Melanerpes formicivorus), helper males have a large positive effect on fledging success in good acorn crop years but only a small positive effect in poor acorn crop years, while helper females exhibit the opposite pattern. Based on these findings, we tested the “concealed helper effects” hypothesis, which proposes that laying females reduce investment in eggs (with respect to their size, number, or quality) in a way that confounds helper effects and results in an absence of a relationship between helpers and breeding success. Results generally failed to support the hypothesis. Mean egg size was positively related to temperatures during the 10 days prior to egg-laying and negatively related to the food supply as indexed by the prior fall’s acorn crop, but there were no significant differences vis-à-vis helpers except for interactions with the acorn crop that only partly corresponded to those predicted. With respect to clutch size, females laid larger clutches when assisted by female helpers, opposite the pattern predicted. Although our results suggest that egg size is adjusted to particular ecological circumstances, we conclude that neither egg nor clutch size is adjusted in a way that confounds the apparent effects of helpers, as proposed by the concealed helper effects hypothesis

Calling where it counts:Subordinate pied babblers target the audience of their vocal advertisements

For territorial group-living species, opportunities to reproduce on the natal territory can be limited by a number of factors including the availability of resources within a territory, access to unrelated individuals, and monopolies on reproduction by dominant group members. Individuals looking to reproduce are therefore faced with the options of either waiting for a breeding opportunity to arise in the natal territory, or searching for reproductive opportunities in non-natal groups. In the cooperatively breeding Southern pied babbler, Turdoides bicolor, most individuals who achieve reproductive success do so through taking up dominant breeding positions within non-natal groups. For subordinate pied babblers therefore, searching for breeding opportunities in non-natal groups is of primary importance as this represents the major route to reproductive success. However, prospecting (where individuals leave the group to search for reproductive opportunities within other groups) is costly and individuals rapidly lose weight when not part of a group. Here we demonstrate that subordinate pied babblers adopt an alternative strategy for mate attraction by vocal advertisement from within their natal territories. We show that subordinates focus their calling efforts on the edges of their territory, and specifically near boundaries with neighbouring groups that have potential breeding partners (unrelated individuals of the opposite sex). In contrast to prospecting, calling individuals showed no body mass loss associated with this behaviour, suggesting that calling from within the group may provide a 'cheap' advertisement strategy. Additionally, we show that subordinates use information regarding the composition of neighbouring groups to target the greatest number of potential mating partners

Human Placental-Specific Epipolymorphism and its Association with Adverse Pregnancy Outcomes

Interindividual variation in DNA-methylation level is widespread in the human genome, despite its critical role in regulating gene expression. The nature of this variation, including its tissue-specific nature, and the role it may play in human phenotypic variation and disease is still poorly characterized. The placenta plays a critical role in regulating fetal growth and development in ways that have lifelong effects on health. To identify genes with a high degree of interindividual DNA methylation variation in the human placenta, we surveyed the human genome using the Illumina GoldenGate Methylation Cancer panel targeting 1505 CpG sites of 807 genes. While many sites show a continuous pattern of methylation levels, WNT2, TUSC3 and EPHB4 were identified to have a polymorphic “on-or-off” pattern of DNA methylation variation at their promoter region which was confirmed by pyrosequencing. Methylation of these genes can be found in 7%–25% of over 100 placentas tested. The methylation state at the promoter of these genes is concordant with mRNA allelic expression. In three informative cases TUSC3 was observed to be methylated on the maternal allele, and it is thus possible this represents a polymorphically imprinted gene. Furthermore, TUSC3 promoter methylation showed evidence for association with preeclampsia. A biological significance of these methylation allelic polymorphisms (MAPs) to human placental diversity is further implied by their placental specificity and absence in mouse. An extended study of blood suggests that MAPs may also be found in other tissues, implicating their utility for tissue-specific association with complex disorders. The identification of such “epipolymorphism” in other tissues and their use in association studies, should improve our understanding of interindividual phenotypic variability and complex disease susceptibility

No behavioural response to kin competition in a lekking species

The processes of kin selection and competition may occur simultaneously if limited individual dispersal i.e. population viscosity, is the only cause of the interactions between kin. Therefore, the net indirect benefits of a specific behaviour may largely depend on the existence of mechanisms dampening the fitness costs of competing with kin. In lekking species, males may increase the mating success of their close relatives (and hence gain indirect fitness benefits) because female prefer large leks. At the same time, kin selection may also lead to the evolution of mechanisms that dampen the costs of kin competition. As this mechanism has largely been ignored to date, we used detailed behavioural and genetic data collected in the black grouse Lyrurus tetrix to test whether males mitigate the costs of kin competition through the modulation of their fighting behaviours according to kinship and the avoidance of close relatives when establishing a lek territory. We found that neighbouring males’ fighting behaviour was unrelated to kinship and males did not avoid settling down with close relatives on leks. As males’ current and future mating success are strongly related to their behaviour on the lek (including fighting behaviour and territory position), the costs of kin competition may be negligible relative to the direct benefits of successful male-male contests. As we previously showed that the indirect fitness benefits of group membership were very limited in this black grouse population, these behavioural data support the idea that direct fitness benefits gained by successful male-male encounters likely outbalance any indirect fitness benefits

The importance of the altricial – precocial spectrum for social complexity in mammals and birds:A review

Various types of long-term stable relationships that individuals uphold, including cooperation and competition between group members, define social complexity in vertebrates. Numerous life history, physiological and cognitive traits have been shown to affect, or to be affected by, such social relationships. As such, differences in developmental modes, i.e. the ‘altricial-precocial’ spectrum, may play an important role in understanding the interspecific variation in occurrence of social interactions, but to what extent this is the case is unclear because the role of the developmental mode has not been studied directly in across-species studies of sociality. In other words, although there are studies on the effects of developmental mode on brain size, on the effects of brain size on cognition, and on the effects of cognition on social complexity, there are no studies directly investigating the link between developmental mode and social complexity. This is surprising because developmental differences play a significant role in the evolution of, for example, brain size, which is in turn considered an essential building block with respect to social complexity. Here, we compiled an overview of studies on various aspects of the complexity of social systems in altricial and precocial mammals and birds. Although systematic studies are scarce and do not allow for a quantitative comparison, we show that several forms of social relationships and cognitive abilities occur in species along the entire developmental spectrum. Based on the existing evidence it seems that differences in developmental modes play a minor role in whether or not individuals or species are able to meet the cognitive capabilities and requirements for maintaining complex social relationships. Given the scarcity of comparative studies and potential subtle differences, however, we suggest that future studies should consider developmental differences to determine whether our finding is general or whether some of the vast variation in social complexity across species can be explained by developmental mode. This would allow a more detailed assessment of the relative importance of developmental mode in the evolution of vertebrate social systems