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

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.

Vocal panting: a novel thermoregulatory mechanism for enhancing heat tolerance in a desert-adapted bird

“…redness of highly vascularised skin patch), that were primarily associated with a thermoregulation function, have then evolved to become visual signals during social displays in some species 53 – 55 . In our study, consistent with previous findings in wild and captive zebra finches 26 , 27 , we showed that heat-calls, starting at T a ~ 41 °C and T b ~ 43 °C, can reliably signal hot environmental conditions and the emitter’s hyperthermic state to embryos (or possibly to conspecifics). Therefore, it is plausible that heat-calls could have evolved from a cue initially associated with a thermoregulatory mechanism into a signal directed at embryos, which increases offspring fitness.…”

“…Audio recordings were analysed visually and audibly in Adobe Audition CC (Creative Cloud 2018) by two researchers who were blind to the respirometry values, behavioural data and air temperatures. The onset of calling corresponded to the time when the bird initiated the first heat-call sequence; and the duration of each sequence was noted as previously described 27 . We calculated the proportion of time spent vocal panting over each T a stage and for the total trial duration.…”

“…This “heat-call” occurs both in wild and captive populations of the Zebra finch ( Taeniopygia guttata ), a common iconic species of the Australian arid interior 29 . Although heat-calling was first discovered during incubation—and found to adaptively program offspring for heat 26 —it is now known, in wild and captive populations, to also be produced spontaneously by heat-stressed adults, even when alone and without an active nest in non-breeding birds 27 . This begs the question as to which other function this peculiar behaviour may fulfil in the emitter, and whether it might be implicated in thermoregulation during acute heat exposure.…”

Acoustic developmental programming: a mechanistic and evolutionary framework

“…Prenatal acoustic information has now been shown to directly and adaptively program individual phenotypes for predicted postnatal environments [7,8]. Far from being passive entities isolated from the external world, it is becoming apparent that embryos survey and respond to their environment so as to direct their development [9,10].…”

Breeding ecology of the Yellow-bellied Warbler (Abroscopus superciliaris)

“…The parent may modify its incubating behavior according to the development of the egg embryo. Several studies have documented parentembryo communication in birds (Colombelli-Négrel et al 2012;Mariette and Buhanan 2016;Katsis et al 2018;Mariette et al 2018). It is possible that A. superciliaris parents can either perceive the progress of embryo development or communicate with the embryo to achieve synchronism.…”