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Hox-logic of body plan innovations for social symbiosis in rove beetles

Joseph Parker, K. Taro Eldredge, Isaiah M. Thomas, Rory Coleman, Steven R. Davis
doi: https://doi.org/10.1101/198945
Joseph Parker
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA
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  • For correspondence: joep@caltech.edu
K. Taro Eldredge
2Department of Ecology and Evolutionary Biology, and Division of Entomology, Biodiversity Institute, University of Kansas, Lawrence, KS, USA
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Isaiah M. Thomas
3Department of Genetics and Development, Columbia University, 701 West 168th Street, New York, NY 10032, USA
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Rory Coleman
4Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA
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Steven R. Davis
5Division of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA
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Abstract

How symbiotic lifestyles evolve from free-living ecologies is poorly understood. In Metazoa’s largest family, Staphylinidae (rove beetles), numerous lineages have evolved obligate behavioral symbioses with ants or termites. Widespread convergence of this lifestyle is thought to stem from a novel, chemically defended body plan that enables free-living species to infiltrate colonies and undergo extreme evolutionary specialization. Here we show how this innovative body plan evolved, via new Hox functions in staphylinids that remodeled the coleopteran groundplan. Using a model staphylinid, Dalotia coriaria, we reveal the Hox basis for changes in thoracic appendage morphology that shortened the beetle elytron and left the abdomen physically unprotected, selecting for an abdominal defense gland that was likely key to unlocking ant and termite societies. We present evidence that the gland evolved through a novel, combinatorial role of the abdominal Hox proteins AbdA and AbdB. These proteins function together to specify distinct gland cell types in neighboring segmental compartments, each cell type synthesizing a different class of compound—irritant, ester and solvent. Only when secreted together do these compounds constitute a bioactive secretion, providing an example of emergent chemical functionality that arises from synergy between individual gland cell types. Hox-controlled specification of glandular diversity implies a modularity in compound biosynthesis that likely catalyzed the evolvability of rove beetle chemistry, including the capacity of symbiotic taxa to produce potent compounds for host deception. This study reveals how Hox-controlled body axis modifications predispose a major animal to convergently evolve into symbionts.

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Posted May 08, 2018.
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Hox-logic of body plan innovations for social symbiosis in rove beetles
Joseph Parker, K. Taro Eldredge, Isaiah M. Thomas, Rory Coleman, Steven R. Davis
bioRxiv 198945; doi: https://doi.org/10.1101/198945
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Hox-logic of body plan innovations for social symbiosis in rove beetles
Joseph Parker, K. Taro Eldredge, Isaiah M. Thomas, Rory Coleman, Steven R. Davis
bioRxiv 198945; doi: https://doi.org/10.1101/198945

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