Prenatal auditory learning in avian vocal learners and non-learners

Abstract

Understanding when learning begins is critical for identifying the factors that shape both the developmental course and the function of information acquisition. Until recently, sufficient development of the neural substrates for any sort of vocal learning to begin in songbirds was thought to be reached well after hatching. New research shows that embryonic gene activation and the outcome of vocal learning can be modulated by sound exposure in ovo . We tested whether avian embryos across lineages differ in their auditory response strength and sound learning in ovo , which we studied in vocal learning (Maluridae, Geospizidae) and vocal non-learning (Phasianidae, Spheniscidae) taxa. While measuring heart rate in ovo , we exposed embryos to (i) conspecific or heterospecific vocalizations, to determine their response strength, and (ii) conspecific vocalizations repeatedly, to quantify cardiac habituation, a form of non-associative learning. Response strength towards conspecific vocalizations was greater in two species with vocal production learning compared to two species without. Response patterns consistent with non-associative auditory learning occurred in all species. Our results demonstrate a capacity to perceive and learn to recognize sounds in ovo , as evidenced by habituation, even in species that were previously assumed to have little, if any, vocal production learning. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Singing on the nest is a widespread behavior in incubating Northern Mockingbirds and increases probability of nest predation

“…Two more potential hypotheses for SOTN are that it is used for song learning and parent identification (reviewed in Haff et al 2015). Traditionally, song learning in birds is thought to occur during a critical period during the late nestling and fledgling stages (Marler and Peters 1981), but growing evidence indicates that developing bird embryos respond to and are shaped by their prenatal acoustic environment (e.g., Katsis et al 2018, Rivera et al 2018, Colombelli-Négrel et al 2021). We found that SOTN rate was significantly higher during the egg stage; however, the role of acoustic signals during the egg stage of mockingbirds remains unstudied and our results suggest this needs further investigation.…”

“…Vocal learning was traditionally thought to occur beginning in the fledgling stage (Marler and Peters 1981); however, a growing body of literature demonstrates that vocal learning begins while developing birds are still in the egg (e.g., Katsis et al 2018, Rivera et al 2018, Colombelli-Négrel et al 2021). We, therefore, predicted that if SOTN functions in vocal learning, then SOTN should occur during both the egg and nestling stages (see Coordination of Parental Care above for details of analysis).…”

Music in Evolution and Evolution in Music

“…If vocal learning were present in the ancestors of birds, one might imagine communities of singing dinosaurs using learned song to defend their territory and to woo their mates. 237 Recent research has suggested that, in some species, this process may even begin in ovo, before hatching (Colombelli-Négrel et al, 2021).…”

Vocal learning in animals and humans

“…It is often assumed that the sensitive period for vocal learning in birds commences sometime after hatching. However, as the paper by Colombelli-Negrel et al [23] makes clear, embryos of various species can perceive and respond to sounds in ovo. The species in the study are few, but highly varied, including a Darwin's finch, two fairy wrens, a penguin and a quail.…”