Regeneration in Reptiles Generally and the New Zealand Tuatara in Particular as a Model to Analyse Organ Regrowth in Amniotes: A Review.

Lorenzo Alibardi,Victor Benno Meyer-Rochow

doi:10.3390/jdb9030036

Lorenzo Alibardi, Victor Benno Meyer-Rochow

Open Access

https://doi.org/10.3390/jdb9030036

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Abstract

The ability to repair injuries among reptiles, i.e., ectothermic amniotes, is similar to that of mammals with some noteworthy exceptions. While large wounds in turtles and crocodilians are repaired through scarring, the reparative capacity involving the tail derives from a combined process of wound healing and somatic growth, the latter being continuous in reptiles. When the tail is injured in juvenile crocodilians, turtles and tortoises as well as the tuatara (Rhynchocephalia: Sphenodon punctatus, Gray 1842), the wound is repaired in these reptiles and some muscle and connective tissue and large amounts of cartilage are regenerated during normal growth. This process, here indicated as “regengrow”, can take years to produce tails with similar lengths of the originals and results in only apparently regenerated replacements. These new tails contain a cartilaginous axis and very small (turtle and crocodilians) to substantial (e.g., in tuatara) muscle mass, while most of the tail is formed by an irregular dense connective tissue containing numerous fat cells and sparse nerves. Tail regengrow in the tuatara is a long process that initially resembles that of lizards (the latter being part of the sister group Squamata within the Lepidosauria) with the formation of an axial ependymal tube isolated within a cartilaginous cylinder and surrounded by an irregular fat-rich connective tissue, some muscle bundles, and neogenic scales. Cell proliferation is active in the apical regenerative blastema, but much reduced cell proliferation continues in older regenerated tails, where it occurs mostly in the axial cartilage and scale epidermis of the new tail, but less commonly in the regenerated spinal cord, muscles, and connective tissues. The higher tissue regeneration of Sphenodon and other lepidosaurians provides useful information for attempts to improve organ regeneration in endothermic amniotes.

Highlights

In order to determine whether cell proliferation is active and regengrow continues in old regenerated tails, we have studied the main sites of proliferation in the three old regenerated tails found in nature and available to us [52,58,59,62] (Figures 8 and 9)
The initial regeneration and tissue organization of the blastema [71], associated with the tuatara’s continuous growth during its lifetime, a feature of its longevity doubted by Dawbin [72], determines the size increases of numerous tissues in the new tail
It can lead to hypertrophy in muscles and growth for the continuous appositional addition of chondroblasts for lengthening the axial cartilage and for the replacement of cartilaginous cells that degenerate during calcification in the central region of the cartilaginous tube [52]

Summary

Focusing on Tail Autotomies in Reptiles

The processes of autotomy and tail regeneration were likely already present in Captorinomorphs [34] before rhynchocephalians like Sphenodon and squamates split apart in the Triassic and these processes were inherited by the two evolutionary lineages of lepidosaurians (Figure 1A) [4]. Regarding convincing evidence that following autotomy regeneration of lost tails in snakes takes place (if it occurs at all), still needs to be presented. It seems that in snakes replacing autotomized tails by functional regenerates either does not happen at all or is very rare and restricted to just some families. In the New Zealand tuatara the phenomenon of replacing a lost tail (or a part of it) does occur This rhynchocephalian reptile with an ancestry dating back over 220 million years, is a species categorised by the Interational Union for the Conservation of Nature (IUCN) as being of “least concern (https://en.wikipedia.org/wiki/Tuatara accessed 28 August 2021). Tissue fixation, embedding, staining, and sectioning techniques have been basically the same in all of our previous investigations involving tuatara as well as other reptiles and detailed descriptions of the histological and ultrastructural preparation methods are given in [42,52]

Tail Regeneration in the Tuatara Represents a Case of Regengrow

Histology of Regenerating and Regenerated Tails in the Tuatara

Findings

Conclusions and Outlook