Evolutionary dynamics of whole-body regeneration across planarian flatworms

Regenerative abilities vary dramatically across animals. Even amongst planarian flatworms, well-known for complete regeneration from tiny body fragments, some species have restricted regeneration abilities while others are almost entirely regeneration incompetent. Here, we assemble a diverse live collection of 40 planarian species to probe the evolution of head regeneration in the group. Combining quantification of species-specific head-regeneration abilities with a comprehensive transcriptome-based phylogeny reconstruction, we show multiple independent transitions between robust whole-body regeneration and restricted regeneration in freshwater species. RNA-mediated genetic interference inhibition of canonical Wnt signalling in RNA-mediated genetic interference-sensitive species bypassed all head-regeneration defects, suggesting that the Wnt pathway is linked to the emergence of planarian regeneration defects. Our finding that Wnt signalling has multiple roles in the reproductive system of the model species Schmidtea mediterranea raises the possibility that a trade-off between egg-laying, asexual reproduction by fission/regeneration and Wnt signalling drives regenerative trait evolution. Although quantitative comparisons of Wnt signalling levels, yolk content and reproductive strategy across our species collection remained inconclusive, they revealed divergent Wnt signalling roles in the reproductive system of planarians. Altogether, our study establishes planarians as a model taxon for comparative regeneration research and presents a framework for the mechanistic evolution of regenerative abilities.

Automated summary

Regenerative abilities vary greatly among planarian species, with some capable of complete regeneration while others are hardly able to regenerate at all. Through experiments and transcriptome-based phylogeny reconstruction, this study reveals multiple independent transitions from robust whole-body regeneration to restricted regeneration in freshwater species. RNA-mediated genetic interference experiments suggest that the Wnt pathway is associated with the emergence of regenerative defects. The study also finds multiple roles of Wnt signalling in the reproductive system of the model species Schmidtea mediterranea, indicating a potential trade-off between egg-laying, asexual reproduction, and Wnt signalling in driving the evolution of regenerative traits.