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Sci Rep
2020 Nov 18;101:20122. doi: 10.1038/s41598-020-77052-8.
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Anatomical and histological analyses reveal that tail repair is coupled with regrowth in wild-caught, juvenile American alligators (Alligator mississippiensis).
Xu C, Palade J, Fisher RE, Smith CI, Clark AR, Sampson S, Bourgeois R, Rawls A, Elsey RM, Wilson-Rawls J, Kusumi K.
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Reptiles are the only amniotes that maintain the capacity to regenerate appendages. This study presents the first anatomical and histological evidence of tail repair with regrowth in an archosaur, the American alligator. The regrown alligator tails constituted approximately 6-18% of the total body length and were morphologically distinct from original tail segments. Gross dissection, radiographs, and magnetic resonance imaging revealed that caudal vertebrae were replaced by a ventrally-positioned, unsegmented endoskeleton. This contrasts with lepidosaurs, where the regenerated tail is radially organized around a central endoskeleton. Furthermore, the regrown alligator tail lacked skeletal muscle and instead consisted of fibrous connective tissue composed of type I and type III collagen fibers. The overproduction of connective tissue shares features with mammalian wound healing or fibrosis. The lack of skeletal muscle contrasts with lizards, but shares similarities with regenerated tails in the tuatara and regenerated limbs in Xenopus adult frogs, which have a cartilaginous endoskeleton surrounded by connective tissue, but lack skeletal muscle. Overall, this study of wild-caught, juvenile American alligator tails identifies a distinct pattern of wound repair in mammals while exhibiting features in common with regeneration in lepidosaurs and amphibia.
Figure 1. Vertebrate appendage regeneration or regrowth is widespread but variable. Schematic summarizing appendage regeneration or regrowth in vertebrates. For mouse, regeneration is only observed in limited tissues, but not in appendages. LB-limb bud.
Figure 2. The original tail is covered in organized scales and caudal vertebrae exhibit prominent structures. Lateral views of original tail segments proximal to the site of injury (a–c). Scales are mottled and organized into transverse rows identified by dorsal scutes. Dorsal views of original tails (d–f). A01 exhibits paired dorsal scutes (d) while A02 and A03 exhibit single dorsal scutes (e,f). Lateral radiographs reveal articulated caudal vertebrae that feature prominent neural spines and hypapophyses (g–i). The last remaining caudal vertebra exhibits bone fissures and lacks vertebral processes. Scale bars are 2.5 cm.
Figure 4. The regrown tail exhibits abnormal scale patterning and lacks caudal vertebrae. Photographs of regrown tail segments after full (a–c) or partial amputation (d) of the posteriortail. The regrown tail lacks dorsal scutes and re-patterned scales are small, black and uniformly distributed. Lateral radiographs demonstrate that caudal vertebrae do not regenerate but are replaced by a rod-like structure (e–h). Superficial samples of the regrown skin stained with Gomori’s Trichrome show all layers of the epidermis and the dermis are present (i). Images are representative and scale bars are 2.5 cm (a–h) or 100 µm (i). ESC epidermal stratum corneum, ESS/B epidermal stratum spinosum/basale, DSL dermal stratum laxum, DSC dermal stratum compactum.
Figure 5. The endoskeleton of the regrown tail forms a hollow, unsegmented rod with randomly distributed foramina. Representative orthogonal magnetic resonance images (a–e) and 3D reconstruction (f) of a regrown alligator tail. The regrown endoskeleton forms a hollow tube that lacks segmentation (a,b). Foramina (b–e) are randomly distributed along the proximo-distal axis of the tail. The regrown endoskeleton is ventrally positioned in the tail (c–f). Scale bars are 2.5 cm.
Figure 6. The endoskeleton of the regrown tail is composed of cartilage.Transverse sections stained with Gomori’s Trichrome (a,b) or subjected to IHC with an anti-collagen type II antibody and counterstained with hematoxylin (c–f). Tissue morphology is cartilage-like, with extensive ECM surrounding round cells in lacunae (black arrowheads), and lacking both vasculature and nerves. Smaller, denser chondrocytes (white arrowhead) are located at the interface between cartilage and the surrounding connective tissue. Images are representative and scale bars are 100 μm.
Figure 8. Anatomical similarities and differences between species capable of appendage regrowth or regeneration. Lateral and transverse schematics of regenerated limbs or tail in alligator, lizard, axolotl, and Xenopus, as well as wound repair in the mouse, are shown on the left. Conserved or divergent features of appendage regeneration or repair relative to the alligator regenerated tail is shown on the right.
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