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A mechanism for punctuating equilibria during mammalian vocal development

Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes (states of equilibrium can be punctuated by sudden change. Here, we studied the early vocal development of three different mammals: common marmoset monkeys, Egyptian fruit bats, and humans. Consis...

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Autores principales: Varella, Thiago T., Zhang, Yisi S., Takahashi, Daniel Y., Ghazanfar, Asif A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232141/
https://www.ncbi.nlm.nih.gov/pubmed/35696441
http://dx.doi.org/10.1371/journal.pcbi.1010173
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author Varella, Thiago T.
Zhang, Yisi S.
Takahashi, Daniel Y.
Ghazanfar, Asif A.
author_facet Varella, Thiago T.
Zhang, Yisi S.
Takahashi, Daniel Y.
Ghazanfar, Asif A.
author_sort Varella, Thiago T.
collection PubMed
description Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes (states of equilibrium can be punctuated by sudden change. Here, we studied the early vocal development of three different mammals: common marmoset monkeys, Egyptian fruit bats, and humans. Consistent with the notion of punctuated equilibria, we found that all three species undergo at least one sudden transition in the acoustics of their developing vocalizations. To understand the mechanism, we modeled different developmental landscapes. We found that the transition was best described as a shift in the balance of two vocalization landscapes. We show that the natural dynamics of these two landscapes are consistent with the dynamics of energy expenditure and information transmission. By using them as constraints for each species, we predicted the differences in transition timing from immature to mature vocalizations. Using marmoset monkeys, we were able to manipulate both infant energy expenditure (vocalizing in an environment with lighter air) and information transmission (closed-loop contingent parental vocal playback). These experiments support the importance of energy and information in leading to punctuated equilibrium states of vocal development.
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spelling pubmed-92321412022-06-25 A mechanism for punctuating equilibria during mammalian vocal development Varella, Thiago T. Zhang, Yisi S. Takahashi, Daniel Y. Ghazanfar, Asif A. PLoS Comput Biol Research Article Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes (states of equilibrium can be punctuated by sudden change. Here, we studied the early vocal development of three different mammals: common marmoset monkeys, Egyptian fruit bats, and humans. Consistent with the notion of punctuated equilibria, we found that all three species undergo at least one sudden transition in the acoustics of their developing vocalizations. To understand the mechanism, we modeled different developmental landscapes. We found that the transition was best described as a shift in the balance of two vocalization landscapes. We show that the natural dynamics of these two landscapes are consistent with the dynamics of energy expenditure and information transmission. By using them as constraints for each species, we predicted the differences in transition timing from immature to mature vocalizations. Using marmoset monkeys, we were able to manipulate both infant energy expenditure (vocalizing in an environment with lighter air) and information transmission (closed-loop contingent parental vocal playback). These experiments support the importance of energy and information in leading to punctuated equilibrium states of vocal development. Public Library of Science 2022-06-13 /pmc/articles/PMC9232141/ /pubmed/35696441 http://dx.doi.org/10.1371/journal.pcbi.1010173 Text en © 2022 Varella et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Varella, Thiago T.
Zhang, Yisi S.
Takahashi, Daniel Y.
Ghazanfar, Asif A.
A mechanism for punctuating equilibria during mammalian vocal development
title A mechanism for punctuating equilibria during mammalian vocal development
title_full A mechanism for punctuating equilibria during mammalian vocal development
title_fullStr A mechanism for punctuating equilibria during mammalian vocal development
title_full_unstemmed A mechanism for punctuating equilibria during mammalian vocal development
title_short A mechanism for punctuating equilibria during mammalian vocal development
title_sort mechanism for punctuating equilibria during mammalian vocal development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232141/
https://www.ncbi.nlm.nih.gov/pubmed/35696441
http://dx.doi.org/10.1371/journal.pcbi.1010173
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