"A young Martian, there can now be no dispute, was really born upon earth during the war, and it was found attached to its parent, partially budded off, just as young lilybulbs bud off, or like the young animals in the fresh-water polyp.
In man, in all the higher terrestrial animals, such a method of increase has disappeared; but even on this earth it was certainly the primitive method. Among the lower animals, up even to those first cousins of the vertebrated animals, the Tunicates, the two processes occur side by side, but finally the sexual method superseded its competitor altogether. On Mars, however, just the reverse has apparently been the case.'" H.G. Wells, The War of the Worlds (1898)
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 vs NED
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.
NED vs No NED
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.
