Many ways to make a novel structure: a new mode of sex comb development in Drosophilidae

Abstract

On macroevolutionary time scales, the same genes can regulate the development of homologous structures through strikingly different cellular processes. Comparing the development of similar morphological traits in closely related species may help elucidate the evolutionary dissociation between pattern formation and morphogenesis. We address this question by focusing on the interspecific differences in sex comb development in Drosophilids. The sex comb is a recently evolved, male-specific structure composed of modified bristles. Previous work in the obscura and melanogaster species groups (Old World Sophophora) has identified two distinct cellular mechanisms that give rise to nearly identical adult morphologies. Here, we describe sex comb development in a species from a more distantly related lineage, the genus Lordiphosa. Although the expression of key regulatory genes is largely conserved in both clades, the cell behaviors responsible for sex comb formation show major differences between Old World Sophophora and Lordiphosa. We suggest that the many-to-one mapping between development and adult phenotype increases the potential for evolutionary innovations.