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

Parker, Joseph and Eldredge, K. Taro and Thomas, Isaiah M. and Coleman, Rory and Davis, Steven R. (2017) Hox-logic of body plan innovations for social symbiosis in rove beetles. . (Unpublished) http://resolver.caltech.edu/CaltechAUTHORS:20181031-101742480

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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.


Item Type:Report or Paper (Discussion Paper)
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https://doi.org/10.1101/198945DOIDiscussion Paper
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission. bioRxiv preprint first posted online Oct. 5, 2017. We thank Brian Spencer (Applied Bionomics, Canada) for providing Dalotia, and Raymond Cloyd (Kansas State University), Graeme Murphy (Ontario Ministry of Food and Agriculture) and Richard Greatrex (Syngenta Bioline, UK) for advice on rearing this species. Yoshinori Tomoyasu provided important feedback on the manuscript. We are grateful to Gary Struhl (Columbia University) in whose laboratory part of this work was carried out. We declare no competing interests.
Subject Keywords:Hox genes, evolution, preadaptations, convergence, symbiosis
Record Number:CaltechAUTHORS:20181031-101742480
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20181031-101742480
Official Citation:Hox-logic of body plan innovations for social symbiosis in rove beetles. Joseph Parker, K. Taro Eldredge, Isaiah Thomas, Rory Coleman, Steven Davis. bioRxiv 198945; doi: https://doi.org/10.1101/198945
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90542
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Nov 2018 17:53
Last Modified:01 Nov 2018 17:53

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