Speculations on the Evolution of Tail Regeneration in Lizards: Lessons from an Outstanding Case of Organ Regeneration in Amniotes

Based on updated information on tail regeneration in lizards, a hypothesis is introduced to explain why these reptiles evolved their regenerative ability. The hypothesis, supported by paleontological evidence, considers tail regeneration associated with autotomy since the Paleozoic in amphibian anthracosaurs of the Carboniferous Period. It is submitted that these ancient amphibians developed tails containing stem cells localized in autotomous planes and/or inter-muscle connective tissues, from which they could regenerate their tails, as some extant salamanders do. The process of stem cell distribution during vertebrate development in salamanders and lizards, however, remains to be demonstrated. It is here suggested that autotomy and regeneration were inherited in the reptiliamorph basal amniotes of the Upper Carboniferous, then in captorhinids of the Permian, in eosuchians of the Triassic, and in the derived Mesozoic lizards, allowing survival and radiation into numerous families. Only in a few lizard families, perhaps under specific ecological adaptations, was autotomy lost, reducing or eliminating tail regeneration. Transcriptome analysis of developing versus regenerating tail indicates numerous differences, suggesting that regeneration utilizes alternative developmental gene pathways from those activated during development. Clarification of gene networks evolved for lizard tail regeneration may indicate the essential steps necessary to regenerate organs also in other amniotes.