Abstract
The evolution of regenerative capacity in multicellular animals represents one of the most complex and intriguing problems in biology. How could such a seemingly advantageous trait as self-repair become consistently attenuated by the evolution? This review article examines the concept of the origin and nature of regeneration, its connection with the processes of embryonic development and asexual reproduction, as well as with the mechanisms of tissue homeostasis. The article presents a variety of classical and modern hypotheses explaining different trends in the evolution of regenerative capacity which is not always beneficial for the individual and notably for the species. Mechanistically, these trends are driven by the evolution of signaling pathways and progressive restriction of differentiation plasticity with concomitant advances in adaptive immunity. Examples of phylogenetically enhanced regenerative capacity are considered as well, with appropriate evolutionary reasoning for the enhancement and discussion of its molecular mechanisms.
Highlights
Animal regeneration is a subject of continuous scientific interest
The problematics of contemporary experimental studies and theoretical investigations in the field have been set up by Weismann (1893, 1899) and Needham (1952). It includes the questions like whether regeneration is a primitive or adaptive trait, what is the role of damage frequency in the evolution of regenerative capacity, what is the role of the environment, what are the reasons for the dynamic evolutionary alterations in regenerative capacity, is it appropriate to consider regeneration as a direct correlate of asexual reproduction, etc
The diversity of cellular mechanisms of blastema formation has been emphasized by Brockes et al whose theory of regeneration origin and evolution is based on two assumptions: (1) regeneration employs the highly conservative principal mechanisms of growth, development, and maintenance of tissue homeostasis universally found in animals, and ensuring the capability of self-repair in certain species/taxa and (2) these highly conservative cellular mechanisms are governed and regulated by a relatively small number of taxon-specific genes responsible for the pronounced regenerative capacity (GarzaGarcia et al, 2010)
Summary
Animal regeneration is a subject of continuous scientific interest. Despite the remarkable progress in the field (Bely and Nyberg, 2010; Zattara et al, 2019), we have to face the fact that regenerative capacity varies colossally among the animal taxa. Despite the enormous amount of experimental data on regeneration, the mechanisms of its evolution remain largely uncertain. The first attempts to understand the laws that drive the evolution of regenerative capacity in animals date to the 19th century. The so-called first rule of regeneration (“the regenerative capacity of animals decreases with an increase in anatomical complexity”) was re-formulated by many authors independently (Vorontsova and Liosner, 1960). The first counterexamples of phylogenetically enhanced regenerative capacity in animals date back to the 19th century as well
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