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Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants

Evolutionary innovations underlie the rise of diversity and complexity—the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mecha...

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Autores principales: Booher, Douglas B., Gibson, Joshua C., Liu, Cong, Longino, John T., Fisher, Brian L., Janda, Milan, Narula, Nitish, Toulkeridou, Evropi, Mikheyev, Alexander S., Suarez, Andrew V., Economo, Evan P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924744/
https://www.ncbi.nlm.nih.gov/pubmed/33651798
http://dx.doi.org/10.1371/journal.pbio.3001031
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author Booher, Douglas B.
Gibson, Joshua C.
Liu, Cong
Longino, John T.
Fisher, Brian L.
Janda, Milan
Narula, Nitish
Toulkeridou, Evropi
Mikheyev, Alexander S.
Suarez, Andrew V.
Economo, Evan P.
author_facet Booher, Douglas B.
Gibson, Joshua C.
Liu, Cong
Longino, John T.
Fisher, Brian L.
Janda, Milan
Narula, Nitish
Toulkeridou, Evropi
Mikheyev, Alexander S.
Suarez, Andrew V.
Economo, Evan P.
author_sort Booher, Douglas B.
collection PubMed
description Evolutionary innovations underlie the rise of diversity and complexity—the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus (Strumigenys), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly.
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spelling pubmed-79247442021-03-10 Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants Booher, Douglas B. Gibson, Joshua C. Liu, Cong Longino, John T. Fisher, Brian L. Janda, Milan Narula, Nitish Toulkeridou, Evropi Mikheyev, Alexander S. Suarez, Andrew V. Economo, Evan P. PLoS Biol Research Article Evolutionary innovations underlie the rise of diversity and complexity—the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus (Strumigenys), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly. Public Library of Science 2021-03-02 /pmc/articles/PMC7924744/ /pubmed/33651798 http://dx.doi.org/10.1371/journal.pbio.3001031 Text en © 2021 Booher et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Booher, Douglas B.
Gibson, Joshua C.
Liu, Cong
Longino, John T.
Fisher, Brian L.
Janda, Milan
Narula, Nitish
Toulkeridou, Evropi
Mikheyev, Alexander S.
Suarez, Andrew V.
Economo, Evan P.
Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title_full Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title_fullStr Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title_full_unstemmed Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title_short Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
title_sort functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924744/
https://www.ncbi.nlm.nih.gov/pubmed/33651798
http://dx.doi.org/10.1371/journal.pbio.3001031
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