Prenatal auditory learning in avian vocal learners and non-learners

Author:

Colombelli-Négrel Diane1,Hauber Mark E.2,Evans Christine1,Katsis Andrew C.1,Brouwer Lyanne345,Adreani Nicolas M.6ORCID,Kleindorfer Sonia16ORCID

Affiliation:

1. College of Science and Engineering, Flinders University, Adelaide 5001, Australia

2. Department of Evolution, Ecology, and Behavior, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

3. Department of Animal Ecology & Physiology, Institute for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands

4. Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

5. Division of Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia

6. Faculty of Life Sciences, University of Vienna, Vienna, Austria

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’.

Funder

USA National Science Foundation

Australian Research Council Discovery Project

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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