Regeneration, the ability to replace lost body structures, and agametic asexual reproduction, such as fission and budding, are post-embryonic developmental trajectories that are widely distributed yet highly variable across the Metazoa. Regeneration capabilities vary dramatically between groups, and agametic reproduction appears strongly associated with high regenerative abilities. The apparent phylogenetic correlation between regeneration and agametic reproduction, along with the extensive developmental similarities between these two processes, suggests that the two are evolutionarily related. However, the directionality leading to this relationship remains unclear: while it has been proposed that regeneration precedes asexual reproduction, the reverse hypothesis has also been proposed. Here, we use a phylogenetically explicit method to formally test these hypotheses in the phylum Annelida, the segmented worms, a group in which regeneration ability is widely variable and in which many species are capable of agametic asexual reproduction by fission. We compiled species-level information on anterior regeneration, posterior regeneration, and fission abilities from the literature, mapped this information onto a phylogenetic tree based on recent molecular studies, and used a Markovian maximum likelihood method to estimate the likelihood of each of these traits being present at each node of the tree. Our results strongly support anterior and posterior regeneration ability being present at the basal node of the annelid tree and being lost 18 and 5 times, respectively, but never re-gained. In contrast, the ability to fission is reconstructed as being absent at the basal node and being gained at least 19 times, with several possible losses. No gain of fission is ever reconstructed to evolve along a branch missing either anterior or posterior regeneration, consistent with the hypothesis that regenerative ability is a requisite to evolving fission.

Supplementary Data Invertebrate Biology 2016 Includes annelid regeneration and fission database (comma separated text table), 2 PDF documents containing field descriptions and full references, 1 Nexus formatted file containing multiple-sequence alignment and RAxML tree, and 1 Geneious formatted file containing multiple-sequence alignment and RAxML tree