Abstract

Songbirds are important models for understanding the mechanisms and fitness consequences of imitative vocal learning. Although the effects of early-life environmental and social conditions on song learning are well-established, the impact of early sound exposure has received surprisingly little attention. Yet recent evidence hints at auditory sensitivity in songbird embryos, including in the zebra finch (Taeniopygia guttata), a classic model species for song learning. Here, we tested whether prenatal exposure to incubation calls—highly rhythmic parental vocalisations produced on the nest—affected song learning in zebra finches. Embryos were exposed in the egg to either incubation (treatment) or contact (control) calls, and after hatching were reared in a large colony. The playback treatment did not affect song complexity nor the accuracy of song copying from the social father, but instead increased learning of non-paternal song syllables. This, in turn, improved males’ mounting success in mating trials. These effects may be attributable to changes in juvenile social behaviours, as playback also influenced male behaviour during mating trials. Our study provides the first experimental evidence that prenatal acoustic environment affects song learning and courtship behaviour in songbirds, thereby raising interesting questions on the role of innate versus acquired biases for vocal learning.

Highlights

  • Songbirds are classic animal models for understanding the neural, social and behavioural processes of imitative vocal learning, which have many striking parallels in human speech[1]

  • In the zebra finch (Taeniopygia guttata), an altricial songbird, ZENK expression in the caudomedial nidopallium was higher in response to rhythmic conspecific songs than to manipulated arrhythmic songs, as early as 15 days post-hatching[28]

  • Treatment and control males did not differ in any acoustic parameters, when considering each parameter singly (Supplementary Table S1) or when parameters were combined into 3 principal components (PCs)

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Summary

Introduction

Songbirds are classic animal models for understanding the neural, social and behavioural processes of imitative vocal learning, which have many striking parallels in human speech[1]. Several recent songbird studies provide evidence that embryos do respond to acoustic stimuli[5,6], and that exposure in ovo to particular conspecific vocalisations, such as parental incubation calls, affects development and postnatal behaviour[7,8], with long-lasting fitness consequences[8]. Classic and more recent imprinting studies in chickens, ducks and quails (which do not sing) show that embryos are sensitive to sound[10], and that hatchlings are more likely to approach or respond vocally to sounds previously heard in the egg[11,12,13] These findings are paralleled in a number of human studies demonstrating that newborns recognise acoustic stimuli that they experienced in utero[14,15]. It remains to be tested whether these effects on growth rate—and later reproductive success—occur directly, or due to changes in vocalisations, including begging calls and perhaps song later in life

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