Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping

Mylene M Mariette,Eve Udino,Alizée Meillère,Andrew E Mckechnie,Rodney N Collins,Andrew T D Bennett,Anaïs Pessato,William A Buttemer,Katherine L Buchanan

doi:10.1038/s41598-018-35853-y

Abstract

Sound is arguably the external cue most accessible to embryos of many species, and as such may constitute an unrivalled source of early information. Recent evidence shows that prenatal sounds, similarly to maternal effects, may shape developmental trajectories. Establishing whether parental vocalisations are signals directed at embryos, or parental cues on which embryos eavesdrop, can elucidate whether parents or embryos control developmental outcomes. Prenatal exposure to a characteristic heat-related parental call was recently shown to alter zebra finch growth and fitness. Here, we test the ecological context of this behaviour in the wild, and assess the information value and specificity of this vocalisation for an embryonic audience. We show that wild zebra finches also produce this characteristic call, only at high temperatures. In addition, in the lab, we demonstrate experimentally that calling is specifically triggered by high air temperatures, can occur without an embryonic audience, and importantly, is predicted by individuals’ body mass. Overall, our findings reveal a specialised heat vocalisation that enables embryonic eavesdropping, by indicating high ambient temperatures, and parents’ capacity to cope with such conditions. This challenges the traditional view of embryos as passive agents of their development, and opens exciting research avenues on avian adaptation to extreme heat.

Highlights

Prenatal acoustic communication occurs in a wide variety of taxa, ranging from crocodiles to humans[1,2,3]
Fluctuating high temperatures trigger in-nest calling in wild zebra finches
Nest-site temperatures tracked ambient temperatures, but were up to 10 °C higher on account of solar radiation, reaching a maximum of 49.9 °C (Fig. 1a). As with their captive counterparts, we found that wild zebra finches under natural field conditions produced a characteristic call at high nest-site temperatures above 35 °C (Est = 3.84, s.e. = 1.07, z = 3.59, P = 0.0003; Fig. 1b)

Summary

Introduction

Prenatal acoustic communication occurs in a wide variety of taxa, ranging from crocodiles to humans[1,2,3]. Prenatal acoustic stimuli alone were recently found to alter post-hatch developmental trajectories and long-term fitness, revealing prenatal communication as a novel mechanism for developmental programming[12]. With few exceptions[19,20], the adaptive value of maternal effects and whether they hinder or facilitate adaptation to rapidly changing environments, remain unclear[17,18,21] This partly reflects the difficulty of establishing whether mothers can actively control hormone and nutrient levels reaching their embryos, in relation to environmental conditions[22,23]. The utterance of parental vocalisations, and their specific environmental triggers and functions, can be readily established experimentally

Methods

Results

Conclusion