Axial regeneration in segmented animals: A post-embryonic reboot of the segmentation process

Abstract

Axial regeneration, the ability to regrow structures along the main body axis, is a widespread, likely ancestral trait of metazoans. Despite its assumed adaptive value, regenerative ability has decreased, disappeared and regained many times during the evolution animal lineages. In most animals capable of regeneration, the process comprises three main stages: wound healing, cell reorganization and morphogenesis of new replacement structures through redeployment of embryonic developmental pathways. Annelids are unique among segmented animals in that many species can regenerate both anterior and posterior ends, rebuilding both terminal, non-segmental tissues and segmental units. Annelid regeneration goes through five main stages: wound healing, blastema formation, blastema differentiation, resegmentation and growth. These five stages involve processes of wound repair, cell migration and proliferation, regeneration of neural and muscular tissues, and generation of segmental structures, along with reorganization of existing tissues to relieve size and position mismatches between the regenerated structures and the stump. During axial regeneration, tissues from non-segmental caps (anterior prostomium or posterior pygidium) form first, and then segmental units are intercalated between the new cap and the stump. Segment formation during anterior regeneration likely involves formation of a transient segment addition zone. In contrast, during posterior regeneration, a new and persistent posterior segment addition zone forms between the pygidium and the stump. While current knowledge of the developmental mechanics and genetics involved in annelid regeneration is still scant, existing data suggest that the process involves redeployment of developmental pathways related to stem and germline cells maintenance, embryogenesis and juvenile/adult posterior growth.