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...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2021-03-01
|
| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001031 |
| _version_ | 1818405844180533248 |
|---|---|
| author | Douglas B Booher Joshua C Gibson Cong Liu John T Longino Brian L Fisher Milan Janda Nitish Narula Evropi Toulkeridou Alexander S Mikheyev Andrew V Suarez Evan P Economo |
| author_facet | Douglas B Booher Joshua C Gibson Cong Liu John T Longino Brian L Fisher Milan Janda Nitish Narula Evropi Toulkeridou Alexander S Mikheyev Andrew V Suarez Evan P Economo |
| author_sort | Douglas B Booher |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T09:02:30Z |
| format | Article |
| id | doaj.art-6ac75a9ea11b49f1888f91cd57f2e890 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-14T09:02:30Z |
| publishDate | 2021-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-6ac75a9ea11b49f1888f91cd57f2e8902022-12-21T23:08:47ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852021-03-01193e300103110.1371/journal.pbio.3001031Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants.Douglas B BooherJoshua C GibsonCong LiuJohn T LonginoBrian L FisherMilan JandaNitish NarulaEvropi ToulkeridouAlexander S MikheyevAndrew V SuarezEvan P EconomoEvolutionary 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.https://doi.org/10.1371/journal.pbio.3001031 |
| spellingShingle | Douglas B Booher Joshua C Gibson Cong Liu John T Longino Brian L Fisher Milan Janda Nitish Narula Evropi Toulkeridou Alexander S Mikheyev Andrew V Suarez Evan P Economo Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants. PLoS Biology |
| 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 |
| url | https://doi.org/10.1371/journal.pbio.3001031 |
| work_keys_str_mv | AT douglasbbooher functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT joshuacgibson functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT congliu functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT johntlongino functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT brianlfisher functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT milanjanda functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT nitishnarula functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT evropitoulkeridou functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT alexandersmikheyev functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT andrewvsuarez functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants AT evanpeconomo functionalinnovationpromotesdiversificationofformintheevolutionofanultrafasttrapjawmechanisminants |