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...
Gespeichert in:
| Veröffentlicht in: | PLoS biology 2021-03, Vol.19 (3), p.e3001031-e3001031 |
|---|---|
| Hauptverfasser: | , , , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | e3001031 |
|---|---|
| container_issue | 3 |
| container_start_page | e3001031 |
| container_title | PLoS biology |
| container_volume | 19 |
| creator | 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 |
| 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. |
| doi_str_mv | 10.1371/journal.pbio.3001031 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_2513695847</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A658713046</galeid><doaj_id>oai_doaj_org_article_6ac75a9ea11b49f1888f91cd57f2e890</doaj_id><sourcerecordid>A658713046</sourcerecordid><originalsourceid>FETCH-LOGICAL-c805t-da6f0b5fdedfdcac3bb860fc406ccbb402ba982876ae93daf2a6189fa9c52dca3</originalsourceid><addsrcrecordid>eNqVk8tuEzEUhkcIREvhDRCMxAYWCb6MPfYGqaooRKqoxG1rnfHYiaMZO9gzAd4ep5lUDeoC5IUv5_v_Yx_rFMVzjOaY1vjtOozRQzffNC7MKUIYUfygOMWsYrNaCPbwzvqkeJLSGiFCJBGPixNKOcO1FKdFvBy9HlzITqXzPmxhtyk3MfRhMKls3dbE5KzT-0CwpQ2xz2w5rExptqEbDwHw5dgNESykoczzZraGn2Vv9Aq8Szca8EN6Wjyy0CXzbJrPim-X779efJxdXX9YXJxfzbRAbJi1wC1qmG1Na1sNmjaN4MjqCnGtm6ZCpAEpiKg5GElbsAQ4FtKC1IxkAT0rXu59N11IaipXUoRhyiUTVZ2JxZ5oA6zVJroe4m8VwKmbgxCXCuLgdGcUB10zkAYwbippsRDCSqxbVltihETZ692UbWx602rjcwW6I9PjiHcrtQxbVUtS1VWVDV5PBjH8GE0aVO-SNl0H3oQx37uSnDCKJMnoq7_Q-183UUvID3DehpxX70zVOWeixhRVPFPze6g8WtM7HbyxLp8fCd4cCTIzmF_DEsaU1OLL5_9gP_07e_39mK32rI4hpWjsbZ0xUrvuOBRE7bpDTd2RZS_u_tGt6NAO9A8fvw2O</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2513695847</pqid></control><display><type>article</type><title>Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><source>Public Library of Science (PLoS)</source><creator>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</creator><creatorcontrib>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</creatorcontrib><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.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3001031</identifier><identifier>PMID: 33651798</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actuation ; Adaptation ; Adaptation, Biological - physiology ; Analysis ; Animals ; Ants ; Ants - metabolism ; Ants - physiology ; Behavior ; Biological Evolution ; Biology and Life Sciences ; Biomechanical Phenomena - physiology ; Biomechanics ; Computer and Information Sciences ; Data collection ; Decision analysis ; Earth Sciences ; Ecology and Environmental Sciences ; Evolution ; Evolution, Molecular ; Evolutionary biology ; Funding ; Innovations ; Jaw ; Mandible - anatomy & histology ; Mandible - physiology ; Medicine and Health Sciences ; Morphology ; Movement ; Muscles ; Phylogenetics ; Phylogeny ; Physiological aspects ; Structure-Activity Relationship ; X-Ray Microtomography - methods</subject><ispartof>PLoS biology, 2021-03, Vol.19 (3), p.e3001031-e3001031</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Booher et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Booher et al 2021 Booher et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c805t-da6f0b5fdedfdcac3bb860fc406ccbb402ba982876ae93daf2a6189fa9c52dca3</citedby><cites>FETCH-LOGICAL-c805t-da6f0b5fdedfdcac3bb860fc406ccbb402ba982876ae93daf2a6189fa9c52dca3</cites><orcidid>0000-0002-4653-3270 ; 0000-0002-8664-6931 ; 0000-0001-7402-0432 ; 0000-0002-0776-4746 ; 0000-0002-8309-8642 ; 0000-0001-5465-0293 ; 0000-0003-4369-1019</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924744/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924744/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33651798$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Booher, Douglas B</creatorcontrib><creatorcontrib>Gibson, Joshua C</creatorcontrib><creatorcontrib>Liu, Cong</creatorcontrib><creatorcontrib>Longino, John T</creatorcontrib><creatorcontrib>Fisher, Brian L</creatorcontrib><creatorcontrib>Janda, Milan</creatorcontrib><creatorcontrib>Narula, Nitish</creatorcontrib><creatorcontrib>Toulkeridou, Evropi</creatorcontrib><creatorcontrib>Mikheyev, Alexander S</creatorcontrib><creatorcontrib>Suarez, Andrew V</creatorcontrib><creatorcontrib>Economo, Evan P</creatorcontrib><title>Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><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.</description><subject>Actuation</subject><subject>Adaptation</subject><subject>Adaptation, Biological - physiology</subject><subject>Analysis</subject><subject>Animals</subject><subject>Ants</subject><subject>Ants - metabolism</subject><subject>Ants - physiology</subject><subject>Behavior</subject><subject>Biological Evolution</subject><subject>Biology and Life Sciences</subject><subject>Biomechanical Phenomena - physiology</subject><subject>Biomechanics</subject><subject>Computer and Information Sciences</subject><subject>Data collection</subject><subject>Decision analysis</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary biology</subject><subject>Funding</subject><subject>Innovations</subject><subject>Jaw</subject><subject>Mandible - anatomy & histology</subject><subject>Mandible - physiology</subject><subject>Medicine and Health Sciences</subject><subject>Morphology</subject><subject>Movement</subject><subject>Muscles</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Structure-Activity Relationship</subject><subject>X-Ray Microtomography - methods</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk8tuEzEUhkcIREvhDRCMxAYWCb6MPfYGqaooRKqoxG1rnfHYiaMZO9gzAd4ep5lUDeoC5IUv5_v_Yx_rFMVzjOaY1vjtOozRQzffNC7MKUIYUfygOMWsYrNaCPbwzvqkeJLSGiFCJBGPixNKOcO1FKdFvBy9HlzITqXzPmxhtyk3MfRhMKls3dbE5KzT-0CwpQ2xz2w5rExptqEbDwHw5dgNESykoczzZraGn2Vv9Aq8Szca8EN6Wjyy0CXzbJrPim-X779efJxdXX9YXJxfzbRAbJi1wC1qmG1Na1sNmjaN4MjqCnGtm6ZCpAEpiKg5GElbsAQ4FtKC1IxkAT0rXu59N11IaipXUoRhyiUTVZ2JxZ5oA6zVJroe4m8VwKmbgxCXCuLgdGcUB10zkAYwbippsRDCSqxbVltihETZ692UbWx602rjcwW6I9PjiHcrtQxbVUtS1VWVDV5PBjH8GE0aVO-SNl0H3oQx37uSnDCKJMnoq7_Q-183UUvID3DehpxX70zVOWeixhRVPFPze6g8WtM7HbyxLp8fCd4cCTIzmF_DEsaU1OLL5_9gP_07e_39mK32rI4hpWjsbZ0xUrvuOBRE7bpDTd2RZS_u_tGt6NAO9A8fvw2O</recordid><startdate>20210302</startdate><enddate>20210302</enddate><creator>Booher, Douglas B</creator><creator>Gibson, Joshua C</creator><creator>Liu, Cong</creator><creator>Longino, John T</creator><creator>Fisher, Brian L</creator><creator>Janda, Milan</creator><creator>Narula, Nitish</creator><creator>Toulkeridou, Evropi</creator><creator>Mikheyev, Alexander S</creator><creator>Suarez, Andrew V</creator><creator>Economo, Evan P</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0002-4653-3270</orcidid><orcidid>https://orcid.org/0000-0002-8664-6931</orcidid><orcidid>https://orcid.org/0000-0001-7402-0432</orcidid><orcidid>https://orcid.org/0000-0002-0776-4746</orcidid><orcidid>https://orcid.org/0000-0002-8309-8642</orcidid><orcidid>https://orcid.org/0000-0001-5465-0293</orcidid><orcidid>https://orcid.org/0000-0003-4369-1019</orcidid></search><sort><creationdate>20210302</creationdate><title>Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants</title><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></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c805t-da6f0b5fdedfdcac3bb860fc406ccbb402ba982876ae93daf2a6189fa9c52dca3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Actuation</topic><topic>Adaptation</topic><topic>Adaptation, Biological - physiology</topic><topic>Analysis</topic><topic>Animals</topic><topic>Ants</topic><topic>Ants - metabolism</topic><topic>Ants - physiology</topic><topic>Behavior</topic><topic>Biological Evolution</topic><topic>Biology and Life Sciences</topic><topic>Biomechanical Phenomena - physiology</topic><topic>Biomechanics</topic><topic>Computer and Information Sciences</topic><topic>Data collection</topic><topic>Decision analysis</topic><topic>Earth Sciences</topic><topic>Ecology and Environmental Sciences</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Evolutionary biology</topic><topic>Funding</topic><topic>Innovations</topic><topic>Jaw</topic><topic>Mandible - anatomy & histology</topic><topic>Mandible - physiology</topic><topic>Medicine and Health Sciences</topic><topic>Morphology</topic><topic>Movement</topic><topic>Muscles</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Physiological aspects</topic><topic>Structure-Activity Relationship</topic><topic>X-Ray Microtomography - methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Booher, Douglas B</creatorcontrib><creatorcontrib>Gibson, Joshua C</creatorcontrib><creatorcontrib>Liu, Cong</creatorcontrib><creatorcontrib>Longino, John T</creatorcontrib><creatorcontrib>Fisher, Brian L</creatorcontrib><creatorcontrib>Janda, Milan</creatorcontrib><creatorcontrib>Narula, Nitish</creatorcontrib><creatorcontrib>Toulkeridou, Evropi</creatorcontrib><creatorcontrib>Mikheyev, Alexander S</creatorcontrib><creatorcontrib>Suarez, Andrew V</creatorcontrib><creatorcontrib>Economo, Evan P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Booher, Douglas B</au><au>Gibson, Joshua C</au><au>Liu, Cong</au><au>Longino, John T</au><au>Fisher, Brian L</au><au>Janda, Milan</au><au>Narula, Nitish</au><au>Toulkeridou, Evropi</au><au>Mikheyev, Alexander S</au><au>Suarez, Andrew V</au><au>Economo, Evan P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2021-03-02</date><risdate>2021</risdate><volume>19</volume><issue>3</issue><spage>e3001031</spage><epage>e3001031</epage><pages>e3001031-e3001031</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33651798</pmid><doi>10.1371/journal.pbio.3001031</doi><orcidid>https://orcid.org/0000-0002-4653-3270</orcidid><orcidid>https://orcid.org/0000-0002-8664-6931</orcidid><orcidid>https://orcid.org/0000-0001-7402-0432</orcidid><orcidid>https://orcid.org/0000-0002-0776-4746</orcidid><orcidid>https://orcid.org/0000-0002-8309-8642</orcidid><orcidid>https://orcid.org/0000-0001-5465-0293</orcidid><orcidid>https://orcid.org/0000-0003-4369-1019</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1545-7885 |
| ispartof | PLoS biology, 2021-03, Vol.19 (3), p.e3001031-e3001031 |
| issn | 1545-7885 1544-9173 1545-7885 |
| language | eng |
| recordid | cdi_plos_journals_2513695847 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | Actuation Adaptation Adaptation, Biological - physiology Analysis Animals Ants Ants - metabolism Ants - physiology Behavior Biological Evolution Biology and Life Sciences Biomechanical Phenomena - physiology Biomechanics Computer and Information Sciences Data collection Decision analysis Earth Sciences Ecology and Environmental Sciences Evolution Evolution, Molecular Evolutionary biology Funding Innovations Jaw Mandible - anatomy & histology Mandible - physiology Medicine and Health Sciences Morphology Movement Muscles Phylogenetics Phylogeny Physiological aspects Structure-Activity Relationship X-Ray Microtomography - methods |
| title | Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T19%3A10%3A20IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Functional%20innovation%20promotes%20diversification%20of%20form%20in%20the%20evolution%20of%20an%20ultrafast%20trap-jaw%20mechanism%20in%20ants&rft.jtitle=PLoS%20biology&rft.au=Booher,%20Douglas%20B&rft.date=2021-03-02&rft.volume=19&rft.issue=3&rft.spage=e3001031&rft.epage=e3001031&rft.pages=e3001031-e3001031&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.3001031&rft_dat=%3Cgale_plos_%3EA658713046%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2513695847&rft_id=info:pmid/33651798&rft_galeid=A658713046&rft_doaj_id=oai_doaj_org_article_6ac75a9ea11b49f1888f91cd57f2e890&rfr_iscdi=true |