The return to water in ancestral Xenopus was accompanied by a novel mechanism for producing and shaping vocal signals

Author:

Kwong-Brown Ursula1ORCID,Tobias Martha L1,Elias Damian O2,Hall Ian C1,Elemans Coen PH3ORCID,Kelley Darcy B1ORCID

Affiliation:

1. Department of Biological Sciences, Columbia University, New York, United States

2. Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, United States

3. Department of Biology, University of Southern Denmark, Campusvej, Denmark

Abstract

Listeners locate potential mates using species-specific vocal signals. As tetrapods transitioned from water to land, lungs replaced gills, allowing expiration to drive sound production. Some frogs then returned to water. Here we explore how air-driven sound production changed upon re-entry to preserve essential acoustic information on species identity in the secondarily aquatic frog genus Xenopus. We filmed movements of cartilage and muscles during evoked sound production in isolated larynges. Results refute the current theory for Xenopus vocalization, cavitation, and favor instead sound production by mechanical excitation of laryngeal resonance modes following rapid separation of laryngeal arytenoid discs. Resulting frequency resonance modes (dyads) are intrinsic to the larynx rather than due to neuromuscular control. Dyads are a distinctive acoustic signature. While their component frequencies overlap across species, their ratio is shared within each Xenopus clade providing information on species identity that could facilitate both conspecific localization and ancient species divergence.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter</xref>).

Funder

Amgen Foundation

National Institutes of Health

Charles H. Revson Foundation

Carlsbergfondet

Det Frie Forskningsråd, Natur og Univers

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference35 articles.

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2. Premotor neuron divergence reflects vocal evolution;Barkan;The Journal of Neuroscience,2018

3. Sexually differentiated, androgen-regulated, larynx-specific myosin heavy-chain isoforms in Xenopus tropicalis; comparison to Xenopus laevis;Baur;Development Genes and Evolution,2008

4. Ventilatory mechanisms of the amphibian, Xenopus laevis; the role of the buccal force pump;Brett;The Journal of Experimental Biology,1979

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