Regenerative potential varies along the anterior-posterior axis of the annelid Capitella teleta

Abstract

Regeneration abilities vary among species, but they can also vary within individuals depending on factors such as developmental stage, amputation location and nutritional status. Many annelids (segmented worms) have well-documented cases of regeneration variation along the anterior-posterior (AP) body axis. However, mechanistic explanations for the diverse regeneration outcomes at different amputation positions remain unknown. Capitella teleta is an annelid with robust posterior regeneration ability but lacks anterior regeneration, although anterior regeneration ability has not been rigorously assessed at multiple amputation sites. In this study, we characterize regeneration ability along the AP axis of C. teleta tail fragments by comparing the post-amputation response of tail fragments cut between segments 1 and 2 and tail fragments cut between segments 10 and 11. Through EdU experiments, in situ hybridization assays, and antibody labeling, we demonstrate that the more anterior amputation site proceeds to later stages of regeneration than the posterior amputation site, but regeneration does not go to completion. The distribution of neoblast-like cells after amputation suggests that these cells do not substantially contribute to formation of the anterior-facing blastema in tail fragments with higher inherent regeneration potential. Lastly, we test whether the greater regenerative competence of tail fragments amputated between segments 1 and 2 increases the probability of accomplishing complete posterior regeneration after treatment with CHIR, a Wnt/{beta}-catenin agonist. Regeneration outcomes are comparable following increase in Wnt/{beta}-catenin signaling regardless of amputation position, suggesting that initial regeneration potential is not a limiting factor of successful posterior regeneration. Comparing tissues with different regenerative abilities within an individual organism can elucidate mechanisms underlying regeneration regulation, thereby enabling the prospect of rescuing or increasing regeneration ability in regeneration-deficient tissues.