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

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Regeneration in Reptiles Generally and the New Zealand Tuatara in Particular As a Model to Analyse Organ Regrowth in Amniotes: a Review Journal of Developmental Biology Review Regeneration in Reptiles Generally and the New Zealand Tuatara in Particular as a Model to Analyse Organ Regrowth in Amniotes: A Review Lorenzo Alibardi 1 and Victor Benno Meyer-Rochow 2,3,* 1 Comparative Histolab Padova and Department of Biology, University of Bologna, 40121 Bologna, Italy; [email protected] 2 Agricultural Science and Technology Research Institute, Andong National University, Andong 36729, Korea 3 Department of Ecology and Genetics, Oulu University, SF-90140 Oulu, Finland * Correspondence: [email protected] 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 Citation: Alibardi, L.; and very small (turtle and crocodilians) to substantial (e.g., in tuatara) muscle mass, while most of Meyer-Rochow, V.B. Regeneration in the tail is formed by an irregular dense connective tissue containing numerous fat cells and sparse Reptiles Generally and the New nerves. Tail regengrow in the tuatara is a long process that initially resembles that of lizards (the Zealand Tuatara in Particular as a latter being part of the sister group Squamata within the Lepidosauria) with the formation of an axial Model to Analyse Organ Regrowth in ependymal tube isolated within a cartilaginous cylinder and surrounded by an irregular fat-rich Amniotes: A Review. J. Dev. Biol. connective tissue, some muscle bundles, and neogenic scales. Cell proliferation is active in the apical 2021, 9, 36. https://doi.org/10.3390/ regenerative blastema, but much reduced cell proliferation continues in older regenerated tails, where jdb9030036 it occurs mostly in the axial cartilage and scale epidermis of the new tail, but less commonly in the Academic Editors: Caroline Beck and regenerated spinal cord, muscles, and connective tissues. The higher tissue regeneration of Sphenodon Simon J. Conway and other lepidosaurians provides useful information for attempts to improve organ regeneration in endothermic amniotes. Received: 3 June 2021 Accepted: 27 August 2021 Keywords: reptilia; rhynchocephalia; Squamata; lepidosauria; Sphenodon; tail; autotomy; morpho- Published: 30 August 2021 genesis; microscopy Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction and Overview iations. 1.1. Wound Healing and Regeneration among Reptiles Generally Extant reptiles represent the modern form of the first amniotes that evolved in the Upper Carboniferous-Lower Permian [1,2]. It has been hypothesized that when amniotes evolved a form of direct development, eliminating the larval growth period and metamor- Copyright: © 2021 by the authors. phic phases of their amphibian ancestors, they also lost a number of genes implicated in Licensee MDPI, Basel, Switzerland. regeneration [3]. The evolution of reptiles from a common ancestor of “basal amniotes” This article is an open access article known as cotylosaurs, resulted in amniotes with a direct embryonic development and distributed under the terms and an ectothermic metabolism, initiated in the Upper Carboniferous and the Permian. One conditions of the Creative Commons lineage led to synapsids, with another leading to sauropsids, having already been estab- Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ lished (Figure1A). Among the sauropsids, independent evolutionary lineages separated 4.0/). J. Dev. Biol. 2021, 9, 36. https://doi.org/10.3390/jdb9030036 https://www.mdpi.com/journal/jdb J. Dev. Biol. 2021, 9, x 2 of 21 J. Dev. Biol. 2021, 9, 36 2 of 21 established (Figure 1A). Among the sauropsids, independent evolutionary lineages sep- arated lepidosaurians from testudines and crocodilians already from the Permian/lower lepidosaurians from testudines and crocodilians already from the Permian/lower Triassic, Triassic,and archosaurians and archosaurians eventually eventually gave rise gave to birds rise to in birds the Jurassic. in the Jurassic. Figure 1. (A), Schematic cladogramme indicating the two main amniote radiation paths from basal amniotes, i.e., synapsids-mammals (pink) and sauropsids that include reptiles (green) and birds (light Figureblue). 1. (B (),A), Table Schematic indicating cladogramme the main organindicating and the tissues two undergoingmain amniote wound radiation healing paths with from scarring, basal amniotes,regengrow i.e., and synapsids-mammals heteromorphic regeneration (pink) and in saur differentopsids sub-orders that include of Reptiles. reptiles (green) and birds (light blue). (B), Table indicating the main organ and tissues undergoing wound healing with scarring,Within regengrow the lepidosaurians, and heteromorphic the regenerati widelyon used in different term for sub-orders the lineage of Reptiles. that includes the tuatara and the sister-group of squamates is “Rhynchocephalia” whereas Sphenodontidae refersWithin to just the one lepidosaurians, family within the this widely lineage. used Squamates, term for i.e.,the scaledlineage reptiles, that includes comprising the tuataralizards, and snakes, the sister-group and amphisbaenians, of squamates separated is “Rhynchocephalia” during the Triassic whereas and gave Sphenodonti- rise to reptiles daewhose refers living to just representatives one family oftenwithin retain this alineage. lizard-like Squamates, body form i.e., [4 scaled]. Different reptiles, from com- pisci- prisingform vertebrates, lizards, snakes, where and wounds amphisbaenians, or injuries separated are constantly during bathed the Triassic and flushed and gave by water, rise toin reptiles the terrestrial whose living environment representatives small injuries often re andtain larger a lizard-like wounds—as body form well [4]. as significantDifferent fromlosses pisciform of skin, tailsvertebrates, or limbs—had where wounds to be repaired or injuries quickly are toco avoidnstantly water bathed loss and and flushed microbe byinfections. water, in Scarring,the terrestrial a rapid environment process of healing, small injuries was and and still larger is the wounds—as common outcome well as in significantterrestrial losses vertebrates of skin, [5 ],tails a process or limbs—had likely to to date be repaired back to allquickly Mesozoic to avoid sauropsids water loss and andtherapsid-early microbe infections. mammals, Scarring, especially a rapid in casesprocess that of involved healing, losseswas and of largestill is organs the common such as outcomethe tail orin limbs.terrestrial vertebrates [5], a process likely to date back to all Mesozoic sau- ropsidsAlthough and therapsid-early mentioned asmammals, early as especially 1886 by Gadow in cases [6 ],that regenerative involved losses capabilities of large in organstestudines such andas the crocodilians tail or limbs. are limited, as indicated in Figure1B. Injuries in tortoises affectAlthough primarily mentioned the carapace, as early the legs, as 1886 or the by tail Gadow and can [6], be regenerative the result of attackscapabilities by large in testudinespredators and or rats, crocodilians of encounters are limited, with machinery as indicated such in Figure as cars, 1B. lawn Injuries mowers, in tortoises etc. and af- of fectexposure primarily to fires, the butcarapace, as observations the legs, or on theTerrapene tail and carolina can beby the Howey result & of Roosenburg attacks by[ 7large] and predatorson Trachemys or rats, scripta of encounters elegans by Negriniwith machin et al.ery [8] such show, as wound cars, lawn healing mowers, in chelonians etc. and isof a exposurevery slow to process. fires, but Freshwater as observations and marine on Terrapene turtles are carolina increasingly by Howey at risk & of Roosenburg being damaged [7] andby on ships Trachemys and motor scripta boats. elegans Wound by Negrini healing et andal. [8] repairs show, towound damaged healing horny in chelonians carapaces is in a tortoisesvery slow demonstrate process. Freshwater a certain regenerative and marine capacity turtles [ 9are–12 ]increasingly and that some at abilityrisk of exists being to damagedat least partially by ships replace and motor a lost boats. or damaged Wound tailhealing has beenand repairs reported to bydamaged Davenport horny [13 car-] for Testudo hermanni and Kuchling [14] for Emydura sp. J. Dev. Biol. 2021, 9, 36 3 of 21 Not a great deal of information is available on the duration of the process in chelonians (Figure1B), but in Testudo hermanni it took the tail spur six years to regenerate to a length of 4 mm and required 12 years to reach 8 mm. At that time, it had regained the pattern and colouration typical of the species. A partial recovery over six years of fire-induced damage to the carapace of a Testudo hermanni has been reported by Martinez-Silvestre &
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