The sea spider Pycnogonum litorale overturns the paradigm of the absence of axial regeneration in molting animals

Abstract

Regenerative abilities and their evolution in the different animal lineages have fascinated generations of biologists. While some taxa are capable of restoring entire individuals from small body fragments, others can regrow only specific structures or lack structural regeneration completely. In contrast to many other protostomes, including the segmented annelids, molting animals (Ecdysozoa) are commonly considered incapable of primary body axis regeneration, which has been hypothesized to be linked to the evolution of their protective cuticular exoskeleton. This holds also for the extraordinarily diverse, segmented arthropods. Contradicting this long-standing paradigm, we here show that immatures of the sea spider Pycnogonum litorale reestablish the posterior body pole after transverse amputation and can regrow almost complete segments and the terminal body region, including the hindgut, anus, and musculature. Depending on the amputation level, normal phenotypes or hypomeric six-legged forms develop. Remarkably, also the hypomeric animals regain reproductive functionality by ectopic formation of gonoducts and gonopores. The discovery of such complex regenerative patterns in an extant arthropod challenges the hitherto widely assumed evolutionary loss of axial regeneration during ecdysozoan evolution. Rather, the branching of sea spiders at the base of Chelicerata and their likely ancestral anamorphic development suggests that the arthropod stem species may have featured similar regenerative capabilities. Accordingly, our results provide an incentive for renewed comparative regeneration studies across ecdysozoans, with the aim to resolve whether this trait was potentially even inherited from the protostome ancestor.