Parental developmental experience affects vocal learning in offspring.

Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son's (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father's song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation.

Species-specific song responses emerge as a by-product of tuning to the local dialect.

Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs.1,2,3 Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning4 and to promote learning of population-typical songs.5 These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur.4 In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect.5,6,7 Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings' early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.

Developmental conditions have intergenerational effects on corticosterone levels in a passerine.

The developmental environment can have powerful, canalizing effects that last throughout an animal's life and even across generations. Intergenerational effects of early-life conditions may affect offspring phenotype through changes in the hypothalamic-pituitary-adrenal axis (HPA). However, such effects remain largely untested in altricial birds. Here, we tested the impact of maternal and paternal developmental conditions on offspring physiology and morphology in the zebra finch (Taeniopygia guttata). Specifically, we exposed one generation (F1) to elevated corticosterone (CORT) during development and quantified the impact on offspring (F2) phenotype. We predicted that intergenerational effects would be apparent through effects of parental developmental treatment on offspring body mass, growth, body condition, body composition, and CORT levels. We found an intergenerational impact on CORT levels, such that F2 birds reared by CORT-treated fathers had higher baseline CORT than F2 birds reared by control fathers. This result shows the potential for intergenerational effects on endocrine function, resulting from developmental conditions. We found no effect of parental treatment on F2 body mass, size, or body condition, but we found that the body mass and tarsus length for offspring and parent were correlated. Our study demonstrates the subtle effects of developmental conditions across generations and highlights the importance of distinguishing between maternal and paternal effects when studying intergenerational effects, especially for species with biparental care.