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Comparative Study
. 2007 Jul;211(1):92-103.
doi: 10.1111/j.1469-7580.2007.00745.x. Epub 2007 May 28.

Epidermal differentiation in embryos of the tuatara Sphenodon punctatus (Reptilia, Sphenodontidae) in comparison with the epidermis of other reptiles

L Alibardi  1 , B J Gill
Affiliations
Comparative Study

Epidermal differentiation in embryos of the tuatara Sphenodon punctatus (Reptilia, Sphenodontidae) in comparison with the epidermis of other reptiles

L Alibardi et al. J Anat. 2007 Jul.

Abstract

Studying the epidermis in primitive reptiles can provide clues regarding evolution of the epidermis during land adaptation in vertebrates. With this aim, the development of the skin of the relatively primitive reptile Sphenodon punctatus in representative embryonic stages was studied by light and electron microscopy and compared with that of other reptiles previously studied. The dermis organizes into a superficial and deep portion when the epidermis starts to form the first layers. At embryonic stages comparable with those of lizards, only one layer of the inner periderm is formed beneath the outer periderm. This also occurs in lizards and snakes so far studied. The outer and inner periderm form the embryonic epidermis and accumulate thick, coarse filaments (25-30 nm thick) and sparse alpha-keratin filaments as in other reptiles. Beneath the embryonic epidermis an oberhautchen and beta-cells form small horny tips that represent overlapping borders along the margin of beta-cells that overlap other beta-cells (in a tile-like arrangement). The tips resemble those of agamine lizards but at a small scale, forming a lamellate-spinulated pattern as previously described in adult epidermis. The embryonic epidermis matures by the dispersion of coarse filaments among keratin at the end of embryonic development and is shed around hatching. The presence of these matrix organelles in the embryonic epidermis of this primitive reptile further indicates that amniote epidermis acquired interkeratin matrix proteins early for land adaptation. Unlike the condition in lizards and snakes, a shedding complex is not formed in the epidermis of embryonic S. punctatus that is like that of the adult. Therefore, as in chelonians and crocodilians, the epidermis of S. punctatus also represents an initial stage that preceded the evolution of the shedding complex for moulting.

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Figures

Fig. 1
Fig. 1
Early (a,b), medium (c–e), and late (f,g) embryonic stages of Sphenodon punctatus. (a) Earliest embryonic stage (LH832) with white and mainly smooth skin. Scale bar = 5 mm. (b) Detail of tail skin (LH832) with forming hinge regions among scales (arrows) while finger skin is smooth (arrowhead). Scale bar = 0.5 mm. (c) More advanced, largely scaled but poorly pigmented embryo (LH2470). Claws are well developed (arrows). Scale bar = 5 mm. (d) Detail of scale variation in the tail of LH2470. Shed epidermis at the bottom of this figure may be artefactual. Scale bar = 1 mm. (e) Detail of limb scales of LH2470. Scale bar = 1 mm. (f) Late embryo (LH831) showing nearly complete scalation and pigmentation. Note caudal crest (arrow) and egg tooth (arrowhead). Scale bar = 5 mm. (g) Detail of arm scales (arrow) and ventral scales (arrowhead) with pigmentation. Scale bar = 1 mm. A, arm scale; C, crest; L, lateral scales; V, ventral scales.
Fig. 2
Fig. 2
Histology of early (a–d) and intermediate (e–j) stages of differentiation in the skin of Sphenodon punctatus. (a) Epidermis with flat periderm cells (arrow) and a few suprabasal cells. Scale bar = 30 µm. (b) Mitoses in the periderm (arrow) and suprabasal layer (arrowhead). Scale bar = 30 µm. (c) Nail epidermis with thick embryonic epidermis above basal layer. Scale bar = 30 µm. (d) Stage of symmetric bump of developing tail scale (poorly preserved in this sample) covered by a thin periderm (arrowhead). Scale bar = 30 µm. (e) Asymmetric tail scale at the beginning of formation of beta-cells (arrow) beneath the thin, intensely stained embryonic epidermis. Scale bar = 30 µm. (f) Accumulation of tile-shaped beta-cells beneath the embryonic epidermis (arrow) of the outer scale surface of a tail scale. Scale bar = 30 µm. (g) Detail of the accumulation of beta-cells beneath the compact embryonic epidermis which forms a serrated interface with the dark initial beta-layer beneath (arrow). Scale bar = 15 µm. (h) Detail of the apical part of a scale showing the oberhautchen forming a dark line (arrowheads) beneath the embryonic epidermis. The stratification of beta-cells (arrow) disappears in the inner scale surface and hinge region. Scale bar = 10 µm. (i) Digit scale showing condensation of beta-cells (arrows) and the irregular outline of the oberhautchen (arrowheads). Scale bar = 30 µm. (j) Detail of condensing beta-layer with the condensed oberhautchen (arrowhead). Scale bar = 40 µm. β, beta cells/layer; D, dermis; DD, dense deeper dermis; EE, embryonic epidermis; H, hinge regions; I, inner scale surface; LD, loose superficial dermis; T, scale tip.
Fig. 3
Fig. 3
Histology of intermediate (a–e) and late (f–i) stages of skin differentiation in Sphenodon punctatus. (a) Ventral scale with compact beta-layer beneath fragmented periderm (arrow). Cells of the mesos-layer form a dense line (arrowhead) beneath the beta-layer. Scale bar = 50 µm. (b) Accumulation of thinning mesos-cells (arrowhead) beneath the compact beta layer and the embryonic epidermis (arrow). Scale bar = 15 µm. (c) Detail of outer surface of tail scale showing the stratification of mesos cells beneath the beta-layer (arrowhead). The latter shows incisions corresponding to the denticles in the inner embryonic epidermis. The arrow points to the outer periderm. Scale bar = 15 µm. (d) Detail of hinge region of tail scale showing the stratification of mesos-alpha cells under the corneous layers (arrow). Fusiform fibroblasts (arrowhead) are present beneath the thin epidermis. Scale bar = 10 µm. (e) Digit scale with forming mesos cells (arrowhead) beneath the beta-layer. The arrow indicates the outer periderm. Scale bar = 30 µm. (f) Accumulation of alpha-cells (arrow) beneath the cornified mesos-alpha region. Scale bar = 10 µm. (g) Compacted mesos-alpha region (arrowhead) beneath the thick beta-layer of the central portion of a finger scale outer surface. Scale bar = 30 µm. (h) Part of outer scale surface showing the thick beta-layer beneath the outer and inner periderm. Alpha cells (arrow) are accumulating to thicken the alpha-layer. Scale bar = 40 µm. (i) In the hinge region the beta-layer beneath the periderm (arrow) becomes thin, and remains as oberhautchen. The thick alpha-layer (arrowhead) remains similar to that in other parts of the scale. Scale bar = 10 µm. α, mesos-alpha region; β, beta-layer; EE, embryonic epidermis; H, hinge region; M, mesos cells; P1, outer periderm; P2, inner periderm.
Fig. 4
Fig. 4
Histology of late stages (a,b), juvenile epidermis (c,d) and moults (e,f) of Sphenodon punctatus. (a) Tail scale with pointed marks in the beta-layer (arrow) and thick alpha-layer (arrowhead). The embryonic epidermis is absent (probably artefactually detached). Scale bar = 50 µm. (b) Detail of the tip of a tail scale showing the numerous cell layers of the thick alpha layer (arrow). The beta-layer with superficial marks (arrowhead) is reduced by the scale tip and inner surface. Scale bar = 10 µm. (c) Finger scale of juvenile with differentiating cells of the intermediate region (arrowheads) beneath the alpha-layer. The arrow indicates the compacted intermediate region (the likely plane of shedding). Scale bar = 15 µm. (d) Differentiating cells (arrowheads) of the intermediate region or new beta layer (arrow) beneath the outer alpha-layer. Scale bar = 15 µm. (e) Section of a moult composed of the beta-layer, thin mesos-region and thick alpha-layer. Scale bar = 50 µm. (f) Section of a moult that includes the corneous layers of the hinge region where the beta-layer becomes very thin (as oberhautchen). Scale bar = 30 µm. α, alpha-layer; β, beta-layer; H, hinge region; DD, deep dense dermis; LD, superficial loose dermis; I, inner scale surface; SO, sensory organ.
Fig. 5
Fig. 5
Ultrastructure of embryonic epidermis of an intermediate stage embryo (RE.2223) of Sphenodon punctatus. (a) General view of superficial layers of the epidermis with beta-keratin packets (arrow) accumulating in the first layer of beta-cells beneath the oberhautchen. Scale bar = 1 µm. (b) Condensation of coarse filaments (arrowheads) in outer and inner periderm, where the cornified cell membrane is visible (double arrowhead). Oberhautchen cells accumulate pale beta-keratin packets (double arrowheads) and some dense bodies (arrows). Scale bar = 0.5 µm. (c) Condensed oberhautchen cell (arrow) with pycnotic nucleus beneath cornified inner and outer periderm (with microvilli). Scale bar = 0.5 µm. β, beta cell; Fβ, forming beta-cell; N, nucleus of first layer of beta-cells; Oβ, oberhautchen/beta-cell; P1, outer periderm; P2, inner periderm.
Fig. 6
Fig. 6
Ultrastructure of embryonic epidermis in intermediate stage embryo (RE.2253) of Sphenodon punctatus. (a) Detail of mature outer and inner periderm with network of coarse filaments (arrowhead) and cornified cell membrane (arrows). Dense beta-packets are condensed in the oberhautchen cells beneath. Scale bar = 0.5 µm. (b) Detail of pointed fold (arrowhead) of oberhautchen cells merged with the underlined beta-layer (the inner periderm has been detached). Arrows indicate beta-keratin bundles. Scale bar = 0.5 µm. (c) Detail of beta-keratin packets (double arrowhead) accumulating into the tip of an oberhautchen fold, which is surrounded by fibrous material (arrows) of inner periderm. Arrowheads on dense granules. Scale bar = 0.5 µm. (d) Detail of pointed tip of oberhautchen cell surrounded by fibrous material (arrows) in the cytoplasm of inner periderm cell. The arrowhead indicates a dense granule. The double arrowhead indicates dense beta-packets. Scale bar = 0.5 µm. K, keratin material; Oβ, oberhautchen/beta-cell; P1, outer periderm; P2, inner periderm; N, nucleus (remnants) of oberhautchen cell; TF, tip of the oberhautchen fold.
Fig. 7
Fig. 7
Schematic drawing of stages of epidermal stratification during embryogenesis (a–f), hatching (dashes between f and g), and post-hatching (g,h) until shedding (i). α, alpha-layer; B, basal epidermal cells; BM, basement membrane; β, beta-layer; CIR, cornified intermediate region (part of it is lost at sloughing of the outer epidermal generation); D, differentiating alpha-layer; Dβ, differentiating beta-layer; DM, differentiating mesos layer; DSL, differentiating shedding line; DT, denticles of maturing embryonic epidermis (dotted); EE, embryonic epidermis (made of outer and inner periderm); IR, spiny-cells of the intermediate region (= oberhautchen cells containing dense granules); M, flat mesos cells; MO, moult; Oβ, oberhautchen/beta-cell (containing dense granules); OT, oberhautchen/beta-cell tips; OV, overlapping borders of oberhautchen/beta-cells; P, periderm; P1, outer periderm; P2, inner periderm; SEE, shed embryonic epidermis; SL, shedding line.
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References

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