Two sets of wing homologs in the crustacean, Parhyale hawaiensis

Abstract

The origin of insect wings is a biological mystery that has fascinated scientists for centuries. Through extensive investigations performed across various fields, two possible wing origin tissues have been identified; a lateral outgrowth of the dorsal body wall (tergum) and ancestral proximal leg structures1,2. With each idea offering both strengths and weaknesses, these two schools of thought have been in an intellectual battle for decades without reaching a consensus3. Identification of tissues homologous to insect wings from linages outside of Insecta will provide pivotal information to resolve this conundrum. Here, through expression analyses and CRISPR/Cas9-based genome-editing in the crustacean, Parhyale hawaiensis, we show that a wing-like gene regulatory network (GRN) operates both in the crustacean terga and in the proximal leg segments, suggesting that (i) the evolution of a wing-like GRN precedes the emergence of insect wings, and (ii) that both of these tissues are equally likely to be crustacean wing homologs. Interestingly, the presence of two sets of wing homologs parallels previous findings in some wingless segments of insects, where wing serial homologs are maintained as two separate tissues4-7. This similarity provides crucial support for the idea that the wingless segments of insects indeed reflect an ancestral state for the tissues that gave rise to the insect wing, while the true insect wing represents a derived state that depends upon the contribution of two distinct tissues. These outcomes point toward a dual origin of insect wings, and thus provide a crucial opportunity to unify the two historically competing hypotheses on the origin of this evolutionarily monumental structure.