Regeneration, Fission and the Evolution of Developmental Novelty in Naid Annelids

Abstract

Regeneration of lost structures and asexual reproduction by fission are post-embryonic trajectories related at the evolutionary and developmental levels. Their phylogenetic distribution within Metazoa has led to the hypothesis that fission can evolve by co-opting regenerative abilities. Fission has evolved multiple times within Annelida, including independent origins at the base of the Pristininae and Naidinae lineages of naid worms. Naids are thus a great system to study the evolution of developmental trajectories of regeneration and fission and their mutual physiological interactions. I made a comparative study of morphogenesis during regeneration and fission in a representative species, <italic>Pristina leidyi</italic> Smith (Pristininae), to test the hypothesis that both trajectories are closely linked by common origin, yet have undergone functional divergence; results show that regeneration and fission share numerous, sometimes exclusive developmental processes, but also present a number of differences spread out along their trajectories. I also examined cell proliferation and growth patterns in <italic>P. leidyi</italic> to characterize the resource allocation strategies it uses to integrate multiple developmental trajectories. I found evidence for a non-linear antero-posterior gradient in proliferation potential and clear interactions between regeneration and fission that strongly depend on fission stage and what body part is lost; similar interactions have been described for naidine annelids and turbellarian flatworms representing independent origins of fission, indicating convergence of fission-associated allocation strategies. I then extended the fission-regeneration comparative study in <italic>P. leidyi</italic> to additional annelids, describing and comparing regeneration and fission in another pristinine, seven naidine and one outgroup species, and found very similar regeneration trajectories among all of them, along with striking levels of convergence of paratomic fission trajectories. Despite similarities, the two paratomic clades presented a distinctive mode of central nervous system development. Finally, I developed novel protocols for dynamic studies of the cellular basis of regeneration, laying groundwork for future comparisons at that level. Altogether, these results strongly support that fission originated multiple times by co-option of regenerative abilities; furthermore, convergence of fission trajectories and resource allocation strategies suggests that similar developmental capabilities, functional constraints and ecophysiological contexts can channel evolutionary trajectories into parallel paths, both in close and distant lineages.