Annelids as models of germ cell and gonad regeneration

Abstract

Germ cells (reproductive cells and their progenitors) give rise to the next generation in sexually reproducing organisms. The loss or removal of germ cells often leads to sterility in established research organisms such as the fruit fly, nematodes, frog, and mouse. The failure to regenerate germ cells in these organisms reinforced the dogma of germline–soma barrier in which germ cells are set‐aside during embryogenesis and cannot be replaced by somatic cells. However, in stark contrast, many animals including segmented worms (annelids), hydrozoans, planaria, sea stars, sea urchins, and tunicates can regenerate germ cells. Here I review germ cell and gonad regeneration in annelids, a rich history of research that dates back to the early 20th century in this highly regenerative group. Examples include annelids from across the annelid phylogeny, across developmental stages, and reproductive strategies. Adult annelids regenerate germ cells as a part of regeneration, grafting, and asexual reproduction. Annelids can also recover germ cells after ablation of germ cell progenitors in the embryos. I present a framework to investigate cellular sources of germ cell regeneration in annelids, and discuss the literature that supports different possibilities within this framework, where germ–soma separation may or may not be preserved. With contemporary genetic‐lineage tracing and bioinformatics tools, and several genetically enabled annelid models, we are at the brink of answering the big questions that puzzled many for over more than a century.

The cost and payout of age on germline regeneration and sexual maturation inPlatynereis dumerilii

“…Many annelids, including P. dumerilii can regenerate germ cells and gonads (Özpolat, 2023). While there have been anecdotal notes on P. dumerilii’ s ability to regenerate its germline during posterior regeneration (Hauenschild and Fischer, 1969; Rebscher, 2014), systematic studies on this process to see whether removal and regeneration of germ cells have an impact on fertility and fecundity have not been carried out before.…”

“…Many annelids express germline/multipotency genes such as vasa, piwi, nanos in tissues that are not strictly germline (Gazave et al, 2013;Kostyuchenko and Smirnova, 2023;Özpolat andBely, 2016, 2015;Planques et al, 2018). For example, in P. dumerilii, vasa is expressed not only in the gonial tissues, but also in the posterior growth zone, and in the regeneration blastema.…”