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"There are colonies of pelagic tunicates which have taken shape like the finger of a glove. Each member of the colony is an individual animal, but the colony is another individual animal, not at all like the sum of its individuals... So a man of individualistic reason, if he must ask, 'Which is the animal, the colony or the individual?' must abandon his particular kind of reason and say, 'Why, it's two animals and they aren't alike in any more than the cells of my body are like me. I am much more than the sum of my cells, and, for all I know, they are much more than the division of me.'"                                                                                                                         John Steinbeck, The Log from the Sea of Cortez

An evo-devo approach to regeneration...

Understanding the ability to regenerate organs and tissues is the long-term goal of research into stem cell biology and regenerative medicine. This is particularly interesting in light of the lack of conservation of regenerative capabilities during evolution: a salamander can regenerate an amputated limb but a human cannot. However, despite the conservation of some molecular mechanisms, it is now clear that different taxa adopt different molecular and cellular strategies to rebuild their lost structures and the evidence against a universal and conserved program behind regeneration is compelling. The term regeneration is in fact a label attached to many different molecular and cellular phenomena that cover an extensive and heterogeneous array of processes present in metazoans and have the common result of restoring, partially or totally, a lost body part.

To better understand the cellular and molecular mechanisms of regeneration and at the same time to attempt to track their evolution. We propose first (1) to focus in conserved chronological steps that occur during the restoration of a particular structure, particularly on the nature and mobilization of the cell precursors; (2) to compare them in a restrained taxonomical clade and (3) to include in the comparison species with different or no regenerative capabilities.

…And tunicates as a playground for experimental evo-devo

Tunicates (Phylum Chordata) encompass a large group of ubiquitous and diverse animals that occupy a wide variety of marine habitats and ecosystems around the world. They are also the closest relative to vertebrates that have extraordinary abilities to regenerate their whole body. For instance, within the family of Styelidae, it possible to find solitary species that reproduce strictly sexually and have limited regenerative capabilities, and colonial species, which can reproduce both sexually and asexually via diverse modes of budding and also evolved tremendous ability to regenerate after injury. Budding and regeneration are two processes of “non-embryonic development” (NED) that involve common cellular and molecular mechanisms.

The discipline of evolutionary developmental biology (evo‐devo) is based on comparisons of developmental mechanisms among species to explore the phenotypic changes during evolution. Tunicates provide different levels in which these comparisons can be explored:

NED vs embryogenesis
Despite being extremely different, in many tunicate budding and sexual development lead to similar post-metamorphic body plans. Then, embryogenesis, metamorphoses, and non-embryonic development can be analyzed side‐by‐side in the same species to explore how homologous features can be obtained following completely different developmental mechanisms.

NED modes are diverse among tunicate species, in terms of the nature of triggering cells and tissues and early ontogenesis. The comparisons between similar and different NED modes in diverse species, or even different NED modes in the same species may illuminate deep homologies in budding mechanisms.

The multiple gains and losses of budding in tunicates provide an opportunity to explore the mechanisms underlying the acquisition of NED.

Two major challenges of regenerative biology concern the rebuilding of not only simple tissues but also complex structures (i.e. with multiple cell and tissue types, axes organization, or sophisticated morphologies) and the lack of conservation of such regenerative capabilities in mammals and particularly in human. The combination of transcriptomic and functional approaches in comparing NED and an evolutionary understanding of asexual development and whole-body regeneration in the sister group of vertebrates has the potential to unravel the bases of developmental plasticity of stem cell and cell de/transdifferentiation in our own phylum.

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