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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 non-kin, 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 towards kin.

N.J.B. was funded by a Netherlands Organisation for Scientific Research Rubicon Fellowship during the experimental phase of this study and by a Royal Society Dorothy Hodgkin Fellowship during the write-up. K.A.S. was funded by a BBSRC David Phillips Research Fellowship during the experimental phase. C.N.T. was supported by an NERC Postdoctoral Fellowship during the experimental phase of the study. D.R.F. was funded by the Max Planck Society and received additional funding from the Deutsche Forschungsgemeinschaft (FA 1420/4-1). The use of information provided by others is a common short-cut adopted to inform decision-making. However, instead of indiscriminately copying others, animals are often selective in what, when and whom they copy. How do they decide which 'social learning strategy' to use? Previous research indicates that stress hormone exposure in early life may be important: while juvenile zebra finches copied their parents' behaviour when solving novel foraging tasks, those exposed to elevated levels of corticosterone (CORT) during development copied only unrelated adults. Here, we tested whether this switch in social learning strategy generalizes to vocal learning. In zebra finches, juvenile males often copy their father's song; would CORT-treated juveniles in free-flying aviaries switch to copying songs of other males? We found that CORT-treated juveniles copied their father's song less accurately as compared to control juveniles. We hypothesized that this could be due to having weaker social foraging associations with their fathers, and found that sons that spent less time foraging with their fathers produced less similar songs. Our findings are in line with a novel hypothesis linking early-life stress and social learning: early-life CORT exposure may affect social learning indirectly as a result of the way it shapes social affiliations. This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'. Publisher PDF

Cultural traditions have been observed in a wide variety of animal species. It remains unclear, however, what is required for social learning to give rise to stable traditions: what level of precision and what learning strategies are required. We address these questions by fitting models of cultural evolution to learned bird song. We recorded 615 swamp sparrow (Melospiza georgiana) song repertoires, and compared syllable frequency distributions to the output of individual-based simulations. We find that syllables are learned with an estimated error rate of 1.85% and with a conformist bias in learning. This bias is consistent with a simple mechanism of overproduction and selective attrition. Finally, we estimate that syllable types could frequently persist for more than 500 years. Our results demonstrate conformist bias in natural animal behaviour and show that this, along with moderately precise learning, may support traditions whose stability rivals those of humans., ‘Conformist bias’, in which individuals learn a common behavioural variant more often than expected by chance, has not been demonstrated convincingly in non-human animals. This study analyses song recordings and models of cultural evolution to show conformist bias in swamp sparrow populations.

That many species of songbirds learn their songs imitatively is well established, but it is less clear why they do so. A component of the developmental-stress hypothesis posits that young males in good condition learn songs more accurately than males in poor condition and that females use learning accuracy as an honest signal of male developmental history. An unresolved problem is how females reliably assess learning accuracy when they are not certain of the identity of the male's tutor and thus the specific model from which a song was copied. We therefore investigated whether song learning accuracy assessment (SLAA) can be reliable, using evolutionary simulation models of song learning. We found that SLAA is indeed less reliable than assessment in which male signals are compared to an unlearned standard, as a result of three types of errors in matching songs to their models. In the simplest models, SLAA was particularly unreliable, but when the model is made more realistic by including features such as geographically constrained learning, repertoire complexity, and, in particular, song categorization, the reliability of SLAA increased. Our results demonstrate a range of conditions under which the assessment of song learning accuracy might be reasonably reliable and therefore likely to evolve.

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart.

Previous studies of learned bird song have suggested the existence of species-universal patterns in song organization: clear clusters in produced songs that do not vary within a species. Here the authors combine a computational method of comparing songs with statistical methods of assessing cluster structure to investigate this issue in a more quantitative manner. The authors first analyze song phonology and then examine song syntax at a population level in 3 species with very different song structure: chaffinches (Fringilla coelebs), zebra finches (Taenopygia guttata), and swamp sparrows (Melospiza georgiana). The authors used a dynamic time-warping algorithm to compare song elements, which closely matched the judgments of human observers. Clustering tendency and validation statistics showed that broad phonological categories existed in all 3 species, but these categories explained no more than half of the overall phonological variation. The authors developed a novel statistic to assess syntactical structure, which indicated that element transitions were not randomly distributed. In the clearest case, in chaffinches, this could be explained by syllables being linked to certain positions within the song. These results demonstrate measures of song organization that can be applied across species, enhancing the potential of comparative studies.

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to possess preference genes that determine which male phenotype they prefer. These rules often do not reflect the mate-choice rules found in empirical studies. In this paper, we compare these two modes of female choice with various types of sexual imprinting. We examine the efficacy of different mate-choice behavior in causing divergence in male traits under simple deterministic one-locus population genetic models as well as under polygenic, individual-based simulations based on the models of Dieckmann and Doebeli (1999). We find that the inheritance mechanism of mate choice can have a large effect on the ease of sympatric speciation. When females imprint on their mothers, the result of the model is similar to phenotype matching, where speciation can occur fairly easily. When females imprint on their fathers or imprint obliquely, speciation becomes considerably less likely. Finally, when females rely on preference genes, male trait evolution occurs easily, but the correlation between trait and preference can be weak, and interpreting these results as speciation may be suspect.

The songs of many birds are unusual in that they serve a role in identifying conspecific mates, yet they are also culturally transmitted. Noting the apparently high rate of diversity in one avian taxon, the songbirds, in which song learning appears ubiquitous, it has often been speculated that cultural transmission may increase the rate of speciation. Here we examine the possibility that song learning affects the rate of allopatric speciation. We construct a population-genetic model of allopatric divergence that explores the evolution of genes that underlie learning preferences (predispositions to learn some songs over others). We compare this with a model in which mating signals are inherited only genetically. Models are constructed for the cases where songs and preferences are affected by the same or different loci, and we analyze them using analytical local stability analysis combined with simulations of drift and directional sexual selection. Under nearly all conditions examined, song divergence occurs more readily in the learning model than in the nonlearning model. This is a result of reduced frequency-dependent selection in the learning models. Cultural evolution causes males with unusual genotypes to tend to learn from the majority of males around them, and thus develop songs compatible with the majority of the females in the population. Unusual genotypes can therefore be masked by learning. Over a wide range of conditions, learning therefore reduces the waiting time for speciation to occur and can be predicted to accelerate the rate of speciation.

In several communication systems that rely on social learning, such as bird song, and possibly human language, the range of signals that can be learned is limited by perceptual biases--predispositions--that are presumably based on genes. In this paper, we examine the coevolution of such genes with the culturally transmitted communication traits themselves, using deterministic population genetic models. We argue that examining how restrictive genetic predispositions are is a useful way of examining the evolutionary origin and maintenance of learning. Under neutral cultural evolution, where no cultural trait has any inherent advantage over another, there is selection in favour of less restrictive genes (genes that allow a wider range of signals to recognized). In contrast, cultural conformity (where the most common cultural trait is favoured) leads to selection in favour of more restrictive genes.

The learned songs of songbirds often cluster into population-wide types. Here, we test the hypothesis that male and female receivers respond differently to songs depending on how typical of those types they are. We used computational methods to cluster a large sample of swamp sparrow ( Melospiza georgiana ) songs into types and to estimate the degree to which individual song exemplars are typical of these types. We then played exemplars to male and female receivers. Territorial males responded more aggressively and captive females performed more sexual displays in response to songs that are highly typical than to songs that are less typical. Previous studies have demonstrated that songbirds distinguish song types that are typical for their species, or for their population, from those that are not. Our results show that swamp sparrows also discriminate typical from less typical exemplars within learned song-type categories. In addition, our results suggest that more typical versions of song types function better, at least in male–female communication. This finding is consistent with the hypothesis that syllable type typicality serves as a proxy for the assessment of song learning accuracy.