Repeated Co-options of Exoskeleton Formation during Wing-to-Elytron Evolution in Beetles

Abstract

The vast diversity in morphology of insect wings provides an excellent model to study morphological evolution. The best-described wing modification is the specification of halteres in Drosophila by a Hox-dependent mechanism, in which a Hox gene affects the expression of genes important for wing development to modify the resulting structure. We have previously shown that highly modified beetle elytra are Hox-free structures despite their divergent morphology, suggesting another mode of evolutionary modification. To understand how elytra have evolved without Hox input, we have analyzed wing development in a coleopteran, Tribolium castaneum. Based on Drosophila mutant phenotypes, we first hypothesized that changes in the wing gene network might have contributed to elytral evolution. However, we found that the wing gene network defined in Drosophila is largely conserved in Tribolium and is also used to pattern the elytra. Instead, we found evidence that the exoskeleton formation has been co-opted downstream of the conserved wing gene network multiple times. We also show evidence that one of these co-options happened prior to the others, suggesting that repeated co-options may have strengthened an advantageous trait. In addition, we found that the Tribolium apterous genes are not only essential for exoskeletalization of the elytra but also are required for the proper identity of the hindwing-an unexpected role that we find to be conserved in Drosophila. Our findings suggest that elytral evolution has been achieved by co-opting a beneficial trait several times while conserving the main framework of wing patterning genes.