TY - JOUR
T1 - A mechanism for punctuating equilibria during mammalian vocal development
AU - Varella, Thiago T.
AU - Zhang, Yisi
AU - Takahashi, Daniel Y.
AU - Ghazanfar, Asif A.
N1 - Funding Information:
This work was supported by an NSF Graduate Fellowship DGE-2039656 (TTV) and NIHNINDS R01NS054898 (AAG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We are very grateful for the comments and suggestions of Talmo Pereira and Marina Wosniack for their thoughtful comments and edits on an earlier draft. Parts of this work were inspired by discussions at the Santa Fe Institute with Eleanor Brush, Jessica Flack and David Krakauer.
Publisher Copyright:
© 2022 Varella et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2022/6
Y1 - 2022/6
N2 - Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes such changes are abrupt: 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.
AB - Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes such changes are abrupt: 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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U2 - 10.1371/journal.pcbi.1010173
DO - 10.1371/journal.pcbi.1010173
M3 - Article
C2 - 35696441
AN - SCOPUS:85133102853
SN - 1553-734X
VL - 18
JO - PLoS computational biology
JF - PLoS computational biology
IS - 6
M1 - e1010173
ER -