A phylum-wide survey reveals multiple independent gains of head regeneration ability in Nemertea

Abstract

Animals vary widely in their ability to regenerate, suggesting that regenerative abilities have a rich evolutionary history. However, our understanding of this history remains limited because regeneration ability has only been evaluated in a tiny fraction of species. Available comparative regeneration studies have identified losses of regenerative ability, yet clear documentation of gains is lacking. We surveyed regenerative ability in 34 species spanning the phylum Nemertea, assessing the ability to regenerate heads and tails either through our own experiments or from literature reports. Our sampling included representatives of the 10 most diverse families and all three orders comprising this phylum. We generated a phylogenetic framework using sequence data to reconstruct the evolutionary history of head and tail regeneration ability across the phylum and found that while all evaluated species can remake a posterior end, surprisingly few could regenerate a complete head. Our analysis reconstructs a nemertean ancestor unable to regenerate a head and indicates at least four separate lineages have independently gained head regeneration ability, one such gains reconstructed as taking place within the last 10-15 mya. Our study highlights nemerteans as a valuable group for studying evolution of regeneration and identifying mechanisms associated with repeated gains of regenerative ability.

Integrative biology of injury in animals

“…The explicit absence of regeneration has also been documented for body parts in numerous animal groups. While regeneration occurs in a broad range of structures across animal phylogeny, current evidence indicates that there have been both evolutionary losses and gains of regeneration ability (Bely & Nyberg, 2010; Bely & Sikes, 2010; Zattara & Bely, 2016; Zattara et al ., 2019). This pattern, alongside comparative descriptions of the molecular, cellular, and morphological features of the regeneration process itself, suggests that instances of regeneration are not necessarily homologous among different lineages (Bely & Nyberg, 2010; Tiozzo & Copley, 2015).…”

“…As with exogenous injury and autotomy, the effects of wound healing and regeneration are often conflated with one another; these are more appropriately considered separate but partly overlapping processes (Brockes & Kumar, 2008; DuBuc, Traylor‐Knowles & Martindale, 2014; Jacyniak et al ., 2017), ones that may even exhibit trade‐offs with one another in some contexts, such as mammals (Wang et al ., 2020). Even different instances of regeneration in diverse species may represent convergent evolution (Bely et al ., 2014; Lai & Aboobaker, 2018; Zattara et al ., 2019), complicating the task of generalizing how and why regeneration evolves and what costs it imposes upon animals. Not only are wound healing and regeneration often not well delineated, but our knowledge of injury responses in general is strongly skewed toward species that can regenerate well, including many which also autotomize their body parts, such as crabs, salamanders, and lizards (Fleming et al ., 2007; Juanes & Smith, 1995; Maginnis, 2006 b ), potentially introducing significant biases.…”

“…However, scar‐free healing can occur even in non‐regenerative contexts [e.g. annelids, nemerteans, arthropods, geckos (Bely, 2010; Bely & Sikes, 2010; Razzell et al ., 2011; Subramaniam, Petrik & Vickaryous, 2018; Townsend et al ., 2017; Zattara et al ., 2019)]. In these cases, larger structures lost to injury may not regenerate, but the wound area does not undergo fibrosis and instead is healed to resemble undamaged surrounding tissue.…”