Understanding how novel structures arise is a central question in evolution. The carapace of the waterflea Daphnia is a bivalved “cape” of exoskeleton that surrounds the animal, and has been proposed to be one of many novel structures that arose through repeated co-option of genes that also pattern insect wings. To determine whether the Daphnia carapace is a novel structure, the expression of pannier, the Iroquois gene aurucan, and vestigial are compared between Daphnia, Parhyale, and Tribolium. The results suggest that the Daphnia carapace did not arise by cooption, but instead represents an elongated ancestral exite (lateral lobe or plate) that emerges from a 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. In addition, the vg-positive region that gives rise to the Daphnia carapace also appears to be present in Parhyale and Tribolium, which do not form a carapace. Thus, rather than a novel structure resulting from gene co-option, the carapace appears to have arisen from an ancient, conserved developmental field that persists in a cryptic state in other arthropod lineages, but in Daphnia became elaborated into the carapace. Cryptic persistence of serially homologous developmental fields may thus be a general solution for the origin of many novel structures.

How to align leg segments between the four groups of arthropods (insects, crustaceans, myriapods, and chelicerates) has tantalized researchers for over a century. By comparing the loss-of-function phenotypes of leg patterning genes in diverged arthropod taxa, including a crustacean, insects, and spiders, we show that all arthropod legs can be aligned in a one-to-one fashion. We propose a model wherein insects incorporated two proximal leg segments into the body wall, which moved the ancestral leg lobe (exite) up onto the back to later form wings. For myriapods and chelicerates with seven leg segments, it appears that one proximal leg segment was incorporated into the body wall. According to this model, the chelicerate exopod and the crustacean exopod emerge from different leg segments, and are therefore proposed to have arisen independently. A framework for how to align arthropod appendages now opens up a powerful system for studying the origins of novel structures, the plasticity of developmental fields, and convergent evolution.