The Daphnia carapace and other novel structures evolved via the cryptic persistence of serial homologs.

Understanding how novel structures arise is a central question in evolution. Novel structures are often defined as structures that are not derived from (homologous to) any structure in the ancestor. The carapace of the crustacean Daphnia magna is a bivalved "cape" of exoskeleton. Shiga et al. proposed that the carapace of crustaceans like Daphnia and many other plate-like outgrowths in arthropods are novel structures that arose through the repeated co-option of genes like vestigial that also pattern insect wings. To determine whether the Daphnia carapace is a novel structure, we compare previous functional work with the expression of genes known to pattern the proximal leg region (pannier, araucan, and vestigial) between Daphnia, Parhyale, and Tribolium. Our results suggest that the Daphnia carapace did not arise by co-option but instead derived from an exite (lateral leg lobe) that emerges from an ancestral proximal leg segment that was incorporated into the Daphnia body wall. The Daphnia carapace, therefore, appears to be homologous to the Parhyale tergal plate and the insect wing. Remarkably, the vestigial-positive tissue that gives rise to the Daphnia carapace appears to be present in Parhyale and Tribolium as a small, inconspicuous protrusion. Thus, rather than a novel structure resulting from gene co-option, the Daphnia carapace appears to have arisen from a shared, ancestral tissue (morphogenetic field) that persists in a cryptic state in other arthropod lineages. Cryptic persistence of unrecognized serial homologs may thus be a general solution for the origin of novel structures.