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

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.

SUBMITTER: Booher DB

PROVIDER: S-EPMC7924744 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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

Booher Douglas B DB Gibson Joshua C JC Liu Cong C Longino John T JT Fisher Brian L BL Janda Milan M Narula Nitish N Toulkeridou Evropi E Mikheyev Alexander S AS Suarez Andrew V AV Economo Evan P EP

PLoS biology 20210302 3

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 diversi ...[more]

PMID: 33651798

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Project description:BackgroundArmy ants are dominant invertebrate predators in tropical and subtropical terrestrial ecosystems. Their close relatives within the dorylomorph group of ants are also highly specialized predators, although much less is known about their biology. We analyzed molecular data generated from 11 nuclear genes to infer a phylogeny for the major dorylomorph lineages, and incorporated fossil evidence to infer divergence times under a relaxed molecular clock.ResultsBecause our results indicate that one subfamily and several genera of dorylomorphs are non-monophyletic, we propose to subsume the six previous dorylomorph subfamilies into a single subfamily, Dorylinae. We find the monophyly of Dorylinae to be strongly supported and estimate the crown age of the group at 87 (74-101) million years. Our phylogenetic analyses provide only weak support for army ant monophyly and also call into question a previous hypothesis that army ants underwent a fundamental split into New World and Old World lineages. Outside the army ants, our phylogeny reveals for the first time many old, distinct lineages in the Dorylinae. The genus Cerapachys is shown to be non-monophyletic and comprised of multiple lineages scattered across the Dorylinae tree. We recover, with strong support, novel relationships among these Cerapachys-like clades and other doryline genera, but divergences in the deepest parts of the tree are not well resolved. We find the genus Sphinctomyrmex, characterized by distinctive abdominal constrictions, to consist of two separate lineages with convergent morphologies, one inhabiting the Old World and the other the New World tropics.ConclusionsWhile we obtain good resolution in many parts of the Dorylinae phylogeny, relationships deep in the tree remain unresolved, with major lineages joining each other in various ways depending upon the analytical method employed, but always with short internodes. This may be indicative of rapid radiation in the early history of the Dorylinae, but additional molecular data and more complete species sampling are needed for confirmation. Our phylogeny now provides a basic framework for comparative biological analyses, but much additional study on the behavior and morphology of doryline species is needed, especially investigations directed at the non-army ant taxa.

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

Publications

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

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