Hox-Mediated Evolution of a Novel Cell Type in Rove Beetles

Author: Kishi, Yuriko

Year: 2027

Degree: Dissertation (Ph.D.)

Advisor: Parker, Joseph

Committee Members: Bronner, Marianne E.; McMahon, Andrew P.; Cai, Long; Parker, Joseph

Option: Biology

DOI: 10.7907/dkx5-hr50

Abstract

Animal body plans are composed of a series of segments, the identities of which are specified early in development by a conserved Hox transcription factor code. How evolution generates new cell types and organs within the context of the bauplan remains incompletely known. Here, we show how canonical Hox proteins can be repurposed as terminal selectors to directly program new cell functions along the body axis. We demonstrate that the insect Hox protein, Abdominal-B (AbdB), has been co-opted from its ancestral role in body axis patterning into a fate-specifying terminal selector in specialized defense gland cells of rove beetles (Staphylinidae). AbdB remains active post-differentiation and instructs the chemical secretion of this cell type by inducing a taxonomically unique gene expression program for toxic benzoquinone biosynthesis. The benzoquinone program is an amalgam of disparate loci, including ancient enzymes from the beetle's primary metabolism and rove beetle-specific paralogs that catalyze critical steps in benzoquinone processing. Persistent AbdB expression drives the activity of this program throughout adult life, sustaining benzoquinone secretion, at least in part by directly activating transcription of program loci. We present evidence that this regulatory innovation has been conserved across 110 million years as these beetles underwent an exceptional radiation, numbering tens of thousands of species. Our findings retrace how new cell- and organ-level properties can originate, via assembly of novel gene expression programs under Hox control.

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