title: Neofunctionalization of embryonic head patterning genes facilitates the positioning of novel traits on the dorsal head of adult beetles.
abstract: The origin and integration of novel traits are fundamental processes during the developmental evolution of complex organisms. Yet how novel traits integrate into pre-existing contexts remains poorly understood. Beetle horns represent a spectacular evolutionary novelty integrated within the context of the adult dorsal head, a highly conserved trait complex present since the origin of insects. We investigated whether otd1/2 and six3, members of a highly conserved gene network that instructs the formation of the anterior end of most bilaterians, also play roles in patterning more recently evolved traits. Using ablation-based fate-mapping, comparative larval RNA interference (RNAi) and transcript sequencing, we found that otd1/2, but not six3, play a fundamental role in the post-embryonic formation of the adult dorsal head and head horns of Onthophagus beetles. By contrast, neither gene appears to pattern the adult head of Tribolium flour beetles even though all are expressed in the dorsal head epidermis of both Onthophagus and Tribolium We propose that, at least in beetles, the roles of otd genes during post-embryonic development are decoupled from their embryonic functions, and that potentially non-functional post-embryonic expression in the dorsal head facilitated their co-option into a novel horn-patterning network during Onthophagus evolution.
authors.affiliation: Department of Biology, Indiana University, 915 East Third Street, Myers Hall 150, Bloomington, IN 47405, USA ezattara@indiana.edu.
authors.forename: Eduardo E
authors.identifier: 0000-0002-9947-9036
authors.initials: EE
authors.lastname: Zattara
authors.affiliation: Department of Biology, Indiana University, 915 East Third Street, Myers Hall 150, Bloomington, IN 47405, USA.
authors.forename: Hannah A
authors.initials: HA
authors.lastname: Busey
authors.affiliation: Department of Biology, Miami University, 700 East High Street, Oxford, OH 45056, USA.
authors.forename: David M
authors.initials: DM
authors.lastname: Linz
authors.affiliation: Department of Biology, Miami University, 700 East High Street, Oxford, OH 45056, USA.
authors.forename: Yoshinori
authors.initials: Y
authors.lastname: Tomoyasu
authors.affiliation: Department of Biology, Indiana University, 915 East Third Street, Myers Hall 150, Bloomington, IN 47405, USA.
authors.forename: Armin P
authors.initials: AP
authors.lastname: Moczek
mesh_terms: D000818:Animals; D019521:Body Patterning / Q000235:genetics*; D001517:Coleoptera / Q000235:genetics* / Q000254:growth & development*; D018507:Gene Expression Regulation, Developmental; D006257:Head / Q000033:anatomy & histology* / Q000196:embryology; D007814:Larva; D010641:Phenotype; D034622:RNA Interference
keywords: co-option; evolutionary novelty; gene function; insect head; post-embryonic development