Linking the genomic signatures of human beat synchronization and learned song in birds

Author:

Gordon Reyna L.123ORCID,Ravignani Andrea4ORCID,Hyland Bruno Julia5,Robinson Cristina M.6ORCID,Scartozzi Alyssa13ORCID,Embalabala Rebecca17ORCID,Niarchou Maria28ORCID,Cox Nancy J.283ORCID,Creanza Nicole236ORCID,

Affiliation:

1. Department of Otolaryngology - Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, TN, USA

2. Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, TN, USA

3. Vanderbilt Brain Institute, Vanderbilt University, Nashville, TN, USA

4. Comparative Bioacoustics Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands

5. Center for Science and Society, Columbia University, New York, NY, USA

6. Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA

7. Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN, USA

8. Division of Genetic Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA

Abstract

The development of rhythmicity is foundational to communicative and social behaviours in humans and many other species, and mechanisms of synchrony could be conserved across species. The goal of the current paper is to explore evolutionary hypotheses linking vocal learning and beat synchronization through genomic approaches, testing the prediction that genetic underpinnings of birdsong also contribute to the aetiology of human interactions with musical beat structure. We combined state-of-the-art-genomic datasets that account for underlying polygenicity of these traits: birdsong genome-wide transcriptomics linked to singing in zebra finches, and a human genome-wide association study of beat synchronization. Results of competitive gene set analysis revealed that the genetic architecture of human beat synchronization is significantly enriched for birdsong genes expressed in songbird Area X (a key nucleus for vocal learning, and homologous to human basal ganglia). These findings complement ethological and neural evidence of the relationship between vocal learning and beat synchronization, supporting a framework of some degree of common genomic substrates underlying rhythm-related behaviours in two clades, humans and songbirds (the largest evolutionary radiation of vocal learners). Future cross-species approaches investigating the genetic underpinnings of beat synchronization in a broad evolutionary context are discussed. This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.

Funder

Vanderbilt University Medical Center

Office of Behavioral and Social Sciences Research

National Science Foundation

National Institute on Deafness and Other Communication Disorders

National Institute of General Medical Sciences

Vanderbilt University

Publisher

The Royal Society

Subject

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

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