Microscopical observations on the regenerating tail in the tuataraSphenodon punctatusindicate a tendency to scarring, but also influence from somatic growth

Abstract

The process of tail regeneration in the tuatara (Sphenodon punctatus) is not entirely known. Similarity to and differences from lizard tail regenerations are indicated in the present histological and ultrastructural study. Regeneration is influenced by the animal's age and ambient temperature, but in comparison to that of lizards it is very slow and tends to produce outgrowths that do not reach the length of the original tail. Although microscopically similar to lizard blastemas, the mesenchyme rapidly gives rise to a dense connective tissue that contains few muscle bundles, nerves, and fat cells. The unsegmented cartilaginous tube forming the axial skeleton is not calcified after 5 months of regeneration, but calcification in the inner region of the cartilage, present after 10 months, increases thereafter. Amyelinic and myelinic peripheral nerves are seen within the regenerating tails of 2–3 mm in length and the spinal cord forms an ependymal tube inside a cartilaginous casing. Tissues of the original tail, like muscles, vertebrae and the adipose mass, are largely replaced by dense connective tissue that occupies most of the volume of the new tail at 5 and 10 months of regeneration. It is unknown whether the differentiation of the dense connective tissue is caused by the relatively low temperature that this species lives under or stems from a genetic predisposition toward scarring as with most other amniotes. Increases of muscle and adipose tissues seen in older regenerated tails derive from somatic growth of the new tail in the years following tail loss and not from a rapid regeneration process like that in lizards.

When one tail isn't enough: abnormal caudal regeneration in lepidosaurs and its potential ecological impacts

“…The rate that lepidosaurs regenerate their tail, and potentially secondary tails, varies dramatically (Arnold, 1984; Maginnis, 2006). Taxa with intra‐vertebral autotomy planes seem to regenerate their tail at a faster rate than those with inter‐vertebral autotomy planes (Arnold, 1984) as do taxa that are short‐lived and early maturing, and those in which the tail has a higher value (Congdon et al ., 1974; Vitt et al ., 1977; Alibardi & Meyer‐Rochow, 1989, 2019). The degree and depth of the wound or break in the tail can also affect the formation and final size of the abnormal regeneration (Woodland, 1920; Simpson, 1964; Alibardi et al ., 1988).…”

“…Tails can affect success in mate signalling and courtship (Hamilton & Sullivan, 2005), mate access and mating success (Salvador, Martin & López, 1995), social status (Fox, Heger & Delay, 1990), conspecific aggression and dominance (Schall et al ., 1989), protection from predators (Bateman, Fleming & Rolek, 2014) and locomotion (McElroy & Bergmann, 2013), as well as being used to store fat and nutrients for energy (Dial & Fitzpatrick, 1981). Tail loss can, therefore, be costly, and energy investment into regeneration and speed of regeneration can affect growth and reproductive output of individuals (Congdon, Vitt & King, 1974; Dial & Fitzpatrick, 1981; Bellairs & Bryant, 1985) and vary dramatically among species, sex and season, and with importance of the tail to the individual's ecology (Congdon et al ., 1974; Vitt, Congdon & Dickson, 1977; Alibardi & Meyer‐Rochow, 1989; Fleming, Valentine & Bateman, 2013; Alibardi & Meyer‐Rochow, 2019).…”

Anatomical and histological analyses reveal that tail repair is coupled with regrowth in wild-caught, juvenile American alligators (Alligator mississippiensis)

“…The absence of skeletal muscle in the regrown alligator tail segment is also observed in the regenerated tuatara tail 44 and in the Xenopus frog forelimb 117 following injury. Moreover, amputation of the Xenopus limb post-metamorphosis (stage 53) results in the formation of a hypomorphic spike composed of an unsegmented cartilage rod that lacks associated skeletal muscle and is surrounded by connective tissue 47 , 117 – 121 .…”

“…For example, Prod1 is involved in cell adhesion and positional identity during limb regeneration, but is specific only to salamanders 40 – 42 . Also lizards, but not the tuatara, are able to regenerate skeletal muscle de novo 3 , 43 , 44 . Regenerative capacity is also contingent upon an animal’s life history traits including body size, growth patterns, life stage, and age 45 .…”

“…While snakes are not known to replace the tail after injury, the tuatara, like lizards, regrows a cartilaginous endoskeleton but exhibits minimal or no skeletal muscle. Rather, the majority of the regrown tuatara tail is composed of dense, connective tissue reminiscent of fibrotic tissue 44 .…”