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

Author:

Booher Douglas B.,Gibson Joshua C.,Liu CongORCID,Longino John T.ORCID,Fisher Brian L.ORCID,Janda Milan,Narula NitishORCID,Toulkeridou EvropiORCID,Mikheyev Alexander S.ORCID,Suarez Andrew V.,Economo Evan P.ORCID

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.

Funder

National Science Foundation

Japan Society for the Promotion of Science

Tinker Foundation

CONACYT

Grantová Agentura České Republiky

Publisher

Public Library of Science (PLoS)

Subject

General Agricultural and Biological Sciences,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Neuroscience

Reference62 articles.

1. Novelty and innovation in the history of life;DH Erwin;Curr Biol,2015

2. Evolution and tinkering;F Jacob;Science,1977

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