Abstract
Regeneration of body structures is an ability widely but unevenly distributed amongst the animal kingdom. Understanding regenerative biology in metazoans means understanding the multiplicity of the cellular and molecular mechanisms that lead to the differentiation, morphogenesis and ultimately the development of a particular regenerating unit. In this manuscript we critically assess the evolutionary considerations suggesting that regeneration is an ancestral trait rather than a mechanism independently evolved in different taxa. As a general method to test evolutionary hypothesis on regeneration, we propose mechanistically dissecting the regenerative processes according to its conserved chronological steps: wound healing, mobilization of cell precursors and morphogenesis. We then suggest interpreting regenerative biology from an evo-devo perspective, proposing a possible theoretical framework and experimental approaches without necessarily invoking a common origin or only multiple losses of regenerative capabilities.
Highlights
On the 25th November 1740, Abraham Trembley first cut a polyp in two, initiating a modern research program on regeneration, a phenomenon that continues to fascinate and mystify today
Understanding regenerative biology in metazoans clearly means understanding the multiplicity of cellular and molecular mechanisms that lead to the activation of progenitor cells, morphogenesis and the development of a particular regenerating unit
We suggest that in a modern context, Morgan’s classical regeneration concepts of epimorphosis and morphallaxis may not be useful if we are trying to find evolutionary relationships among regenerative processes
Summary
On the 25th November 1740, Abraham Trembley first cut a polyp in two, initiating a modern research program on regeneration, a phenomenon that continues to fascinate and mystify today. This trait is mapped onto animal phylogenies as a single character, and its presence in the last common ancestor of animals appears self-evident, with the variability of “regenerative potential” among the animal kingdom typically explained by invoking adaptive mechanisms of its maintenance and secondary loss (Brockes et al, 2001; Brockes and Kumar, 2008; Bely, 2010; Bely and Nyberg, 2010) It is possible, even probable, that the last common ancestor of extant animals possessed some level of broadly defined regenerative ability, and that aspects of the regenerative abilities of contemporary animals are, in some sense, historically continuous with this, the evidence that such a view can be transferred to the level of cellular and molecular mechanisms needs to be critically assessed. We advocate interpreting regenerative biology from an evo-devo perspective; we propose one such framework and experimental approaches
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