Skin morphology of five species of rock lizards of the genus Darevskia (Lacertidae, Squamata)

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The microstructure of the tuberculate dorsal and lamellar ventral skin of the body in rock lizards of different ages (Darevskia raddei, D. nairensis, D. valentini, D. dahli, D. armeniaca) has been described for the first time. The thickness of the skin in the most xerophilic species (D. raddei) is less than that in the more hygrophilic species. Rock lizards have single or paired longitudinal skin folds that are not closed from the side, which stretch along the inner side of the scales to its distal edge. Small folds are also present in the lining of the squamous pocket; they consist of all layers of the skin and subcutaneous tissue. A large fold is able to completely block the cavity of the squamous pocket, the volume of which changes with the contraction of the subcutaneous muscle bundles reaching the bases of the scales. Small folds are also present on the scales of tuberous skin. In hygrophilic lizards (Zootoca vivipara), similar formations appear at later stages of postnatal ontogenesis than in rock lizards. The probable functional significance of the described skin structures is discussed.

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Sobre autores

O. Chernova

A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Autor responsável pela correspondência
Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071

E. Galoyan

A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071

Yu. Ivlev

A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Email: olga.chernova.moscow@gmail.com
Rússia, Moscow, 119071

Bibliografia

  1. Гражданкин А. В. Особенности морфологии кожного покрова наземных рептилий в связи с их терморегуляцией // Зоол. журн. 1974. Т. 53. № 12. С. 1894–1897.
  2. Даревский И. C. Скальные ящерицы Кавказа: Систематика, экология и филогения полиморфной группы кавказских ящериц подрода Archaeolacerta / Зоол. ин-т. Л.: Наука. Ленингр. отд., 1967. 214 с.
  3. Даревский И. С., Гречко В. В., Куприянова Л. A. Ящерицы, размножающиеся без самцов // Природа. 2000. № 9. С. 131–133.
  4. Николаев О. Д., Белова Д. А., Новиковa Б. А., Симисa И. Б., Петросян Р. К., Аракелян М. С., Комарова В. А., Галоян Э. А. Особенности термобиологии партеногенетических скальных ящериц (Darevskia armeniaca и Darevskia unisexualis) и обоеполового вида Darevskia valentini (Lacertidae, Squamata) // Зоол. журн. 2021. Т. 100. № 11. С. 1214–1223. https://doi.org/10.31857/S0044513421090063
  5. Попов В. Л., Механика контактного взаимодействия и физика трения. От нанотрибологии до динамики землетрясений. М.: Физматлит, 2013. 352 с.
  6. Соколов В. Е., Даревский И. С., Котова Е. Л., Чернова О. Ф. Специализированные кожные органы такырной круглоголовки Phrynocephalus helioscopus (Reptilia. Squamata, Agamidae) // Зоол. журн. 1997. Т.70. № 4. С. 466–472.
  7. Соколов В. Е., Котова Е. Л., Чернова O. Ф., 1994. Кожные железы рептилий (Reptilia). Обзор исследований. М.: МЦНЕИ. С. 1–94.
  8. Соколов В. Е., Скурат Л. Н., Степанова Л. В., Шабадаш С. А. Руководство по изучению кожного покрова млекопитающих. М.: Наука, 1988. 278 с.
  9. Abramoff M. D., Magalhaes P. J., Ram S. J. Image Processing with ImageJ // Biophotonics International. 2004. V. 11. № 7. P. 36–42.
  10. Ahmadzadeh F., Flecks M., Carretero M. A., Mozaffari O., Böhme W., Engler J., Harris D. J., IIgaz C., Üzüm. N. Cryptic speciation patterns in Iranian rock lizards uncovered by integrative taxonomy // PloS ONE. 2013. V. 8. № 12. P. 1–17. https://doi.org/10.1371/journal.pone.0080563
  11. Akat E., Pombal V. F., Yenmiş M., Molist P., Megias M., Somuncu S., Vesely M., Anderson R., Ayaz D. Comparison of vertebrate skin structure at class level: A review // Anat. Rec. 2022. V. 305. № 12. P. 3543– 3608. https://doi.org/10.1002/ar.24908
  12. Alibardi L. Scale morphogenesis during embryonic development in the lizard Anolis lineatopus // J. Anat. 1996. V. 188. P. 713–725.
  13. Alibardi L. Morphogenesis of the digital pad lamellae in the embryo of the lizard Anolis lineatopus // J. Zool. 1997. V. 243. P. 47–56. https://doi.org/10.1111/j.1469-7998.1997.tb05755.x
  14. Alibardi L. Ultrastructure of the embryonic snake skin and putative role of histidine in the differentiation of the shedding complex // J. Morphol. 2002. V. 251. P. 149–168. https://doi.org/10.1002/jmor.1080
  15. Alibardi L. Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes // J. Exp. Zool. Part B. Mol. Dev. Evol. 2003. V. 298. № 1. P. 12–41. https://doi.org/10.1002/jez.b.24
  16. Alibardi L. Review: Cell biology of adhesive setae in gecko lizards // Zoology. 2009. V. 112. P. 403–424. https://doi.org/10.1016/j.zool.2009.03.005
  17. Alibardi L. Sauropsids cornification is based on corneous beta-proteins, a special type of keratin-associated corneous proteins of the epidermis // J. Exp. Zool. Part B. Mol. Dev. Evol. 2016. V. 326. № 6. P. 1–14. https://doi.org/10.1002/jez.b.22689
  18. Alibardi L. Keratinization and cornification are not equivalent processes but keratinization in fish and amphibians evolved into cornification in terrestrial vertebrates // Exp. Dermat. 2022. V. 31. № 5. P. 794–799. https://doi.org/10.1111/exd.14525
  19. Alibardi L., Thompson M. B. Epidermal differentiation in the developing scales of embryos of the Australian scincid lizard Lampropholis quicnenoti // J. Morphol. 1999. V. 241. P. 139–152. https://doi.org/10.1002/(SICI)1097-4687(199908)241:2<139::AID-JMOR4>3.0.CO;2-H.
  20. Alibardi L., Toni M., Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales // Prog. Histochem. Cytochem. 2006. V. 40. № 2. P. 73–134. https://doi.org/10.1016/j.proghi.2006.01.001
  21. Ananjeva N. B., Dilmuchamedov M., Matveyeva T. The skin sense organs of some iguanian lizards // J. Herpetol. 1991. V. 25. P. 186–199. https://doi.org/10.2307/1564647
  22. Araya-Donoso R., San Juan E., Tamburrino I., Lamborot M., Veloso C., Véliz D. Integrating genetics, physiology and morphology to study desert adaptation in a lizard species // J. Anim. Ecol. 2022. V. 91. № 6. P. 1148–1162. https://doi.org/10.1111/1365-2656.13546
  23. Arribas O. J. Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertens, 1921, sensu lato) and their relationships among the Eurasian lacertid radiation // Russ. J. Herpetol. 1999. V. 6. № 1. P. 1–22.
  24. Breyer H. Über Hautsinnesorgane und Haftung bei Lacertilien // Zool. Jahr. 1929. Bd. 51. Abt. F. Anatomie. S. 549–581.
  25. Calvaresi M., Eckhart L., Alibardi L. The molecular organization of the beta-sheet region in Corneous betaproteins (beta-keratins) of sauropsids explains its stability and polymerization into filaments // J. Struct. Biol. 2016. V. 194. P. 282–291. https://doi.org/10.1016/j.jsb.2016.03.004
  26. Carver W. S., Sawyer R. H. Development and keratinization of the epidermis in the common lizard, Anolis carolinenesis // J. Exp. Zool. 1987. V. 243. P. 435–443. https://doi.org/ 10.1002/jez.1402430310
  27. Chang Ch., Wu P., Baker R. E., huong Ch.-M. Reptile scale paradigm: Evo-Devo pattern formation and regeneration // Int. J. Dev. Biol. 2009. V. 53. P. 813–826. https://doi.org/10.1387/ijdb.072556cc.
  28. Comans P., Buchberger G., Buchsbaum A., Baumgartner R., Koller A., Bauer S., Baumgartner W. Directional, passive liquid transport: the Texas horned lizard as a model for a biomimetic ‘liquid diode’ // J. R. Soc. Interface. 2015. V. 12. № 109. P. 20150415. https://doi.org/10.1098/rsif.2015.0415
  29. Comans P., Withers P. C., Esser F. J., Baumgartner W. Cutaneous water collection by a moisture-harvesting lizard, the thorny devil (Moloch horridus) // J. Exp. Biol. 2016. V. 219. № 21. P. 3473–3479. https://doi.org/10.1242/jeb.148791
  30. Cox C. L., Cox R. M. Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles // Evolution. 2015. V. 69. № 9. P. 2507–2516.
  31. Dhouailly D. A new scenario for the evolutionary origin of hair, feather, and avian scales // J. Anat. 2009. V. 214. № 4. P. 587−606. https://doi.org/10.1111/j.1469-7580.2008.01041.x.
  32. Dupoué A., Rutschmann A., Le Galliard J. F., Miles D. B., Clobert J., Devardo D. F., Brusch G. A. IV, Meylan S. Water availability and environmental temperature correlate with geographic variation in water balance in common lizards // Oecologia. 2017. V. 185. № 4. P. 561–571. https://doi.org/10.1007/s00442-017-3973-6.
  33. Flaxman B. A. Cell differentiation and its control in the vertebrate epidermis // Integrative and Comparative Biology (ICB). 1972. V. 12. № 1. P. 13−26. https://doi.org/10.1093/icb/12.1.13
  34. Gabelaia M., Adriaens D., Tarkhnishvili D. Phylogenetic signals in scale shape in Caucasian rock lizards (Darevskia species) // Zool. Anz. 2017. V. 268. P. 32–40. https://doi.org/10.1016/j.jcz.2017.04.004
  35. Galoyan E., Moskalenko V., Gabelaia M., Tarkhnishvili D., Spangenverg V. E., Shamkina A., Arakelyan M., Syntopy of two species of rock lizards (Darevskia raddei and Darevskia portschinskii) may not lead to hybridization between them // Zool. Anz. 2020. V. 288. P. 43–52. https://doi.org/10.1016/j.jcz.2020.06.007 https://sev-in.ru/sites/default/files/2023-08/Supplementary_to_Skin_morphology_of_rock_lizards.pdf.
  36. Irish F. J., Williams E. E., Seling E. Scanning electron microscopy of changes in epidermal structure occurring during the shedding cycle in squamate reptiles // J. Morph. 1988. V. 197. № 1. P. 105–126. https://doi.org/10.1002/jmor.1051970108
  37. Kandagel R., Elwan M., Abumdour M. Comparative ultrastructural-functional characterizations of the skin in three reptile species: Chalcides ocellatus, Uromastyx aegyptia aegyptia, and Psammophis schokari aegyptia (Forskål, 1775): Adaptive strategies to their habitat // Microsc. Res. Tech. 2021. V. 84. № 9. P. 1–15. https://doi.org/10.1002/jemt.23766
  38. Kattan G. H., Lillywhite H. B. Humidity acclimation and skin permeability in the lizard Anolis carolinensis // Physiol. Zool. 1989. V. 62. № 2. P. 593–606. https://doi.org/10.1086/physzool.62.2.30156187
  39. Landmann L. The sense organs in the skin of the head of Squamata (Reptilia) // Isr. J. Zool. 1975. V. 24. P. 99–135. https://doi.org/10.1080/00212210.1975.10688416
  40. Landmann L. Epidermis and dermis // Biology of Integument. V. 2. / Eds Bereiter-Hahn J., Matoltsy A. G., Richards K. S. Berlin, Heidelberg: Springer-Verlag, 1986. P. 150–187.
  41. Lillywhite H. B. Plasticity of the water barrier in vertebrate integument // International Congress Series. 2004. V. 1275. P. 283–290.
  42. Lillywhite H. B. Water relations of tetrapod integument // J. Exp. Biol. 2006. V. 209. № 2. P. 202–226. https://doi.org/10.1242/jeb.02007
  43. Maderson P. F. A. Keratinized epidermal derivatives as an aid to climbing in gekkonid lizards // Nature. 1964. V. 203. P. 780−781. https://doi.org/ 10.1038/203780a0
  44. Maderson P. F. A. The structure and development of the squamate epidermis // Biology of the skin and hair growth / Eds Lyne A. G., Short B. F. Sydney: Angus & Robertson, 1965. P.129–153.
  45. Maderson P. F. A. Lizard glands and lizard hands: models for evolutionary study // Forma et Functio. 1970. V. 3. P. 179−204.
  46. Maderson P. F. A. Some developmental problems of the reptilian integument // Biology of the Reptilia / Eds Hans C., Billett F., Maderson P. F.A. . 1985. V. 14. P. 525−598.
  47. Maderson P. F. A., Licht P. Epidermal morphology and sloughing frequency in normal and prolactin treated Anolis carolinensis (Iguanidae, Lacertilia) // J. Morphol. 1967. V. 123. P. 157–172. https://doi.org/10.1002/jmor.1051230205
  48. Mi Ch., Ma L., Wang Y., Wu D., Du W., Sun B. Temperate and tropical lizards are vulnerable to climate warming due to increased water loss and heat stress // Proc. Biol. Sci. 2022. V. 289. № 1980. P. 20221074. https://doi.org/10.1098/rspb.2022.1074
  49. Mittal A. K., Singh J. P. A. Hinge epidermis of Natrix piscator during its sloughing cycle – structural organization and protein histochemistry // J. Zool. 1987. V. 213. № 4. P. 685–695.
  50. Mohammed M. B. H. Skin development in the lizard embryo, Chalcides ocellatus forscae (Scincidae, Sauria, Reptilia) // Wasm. J. Biol. 1987. V. 45. № 1−2. P. 49−58.
  51. Roberts J. B., Lillywhite H. B. Lipid barrier to water exchange in Reptile epidermis // Science. 1980. V. 207. № 4435. P. 1077–1079. https://doi.org/10.1126/science.207.4435.1077
  52. Rutland C. S., Cigler P., Kubale V. Reptilian skin and its special histological structure // Veterinary Anatomy and Physiology / Eds Rutland C. S., Kubale V. IntechOpen. 2019. P. 1–21. www.intecho.com http://dx.doi.org/10.5772/intechopen.84212
  53. Sherbrooke W. C., Scardino A. J., Rocke de Nys, Schwarzkopf L. Functional morphology of hinges used to transport water: Convergent drinking adaptations in desert lizards (Moloch herridus and Phrynosoma cornutum) // Zoomorphology. 2007. V. 126. P. 89–102. https://doi.org/10.1007/s00435-007-0031-7
  54. Swadźba E., Rupik W. Ultrastructural studies of epidermis keratinization in grass snake embryos Natrix natrix L. (Lepidosauria, Serpentes) during late embryogenesis // Zoology. 2010. V. 113. P. 339–360. https://doi.org/10.1016/j.zool.2010.07.002
  55. Yenmiş M., Ayaz D., Sherbrooke W. C., Veselý M. A comparative behavioural and structural study of rain-harvesting and non-rain-harvesting agamid lizards of Anatolia (Turkey) // Zoomorphology. 2016. V. 135. № 1. P. 137–148. https://doi.org/10.1007/s00435-015-0285-4
  56. Žagar A., Vrezec A., Carretero M. A. Do the thermal and hydric physiologies of Zootoca (vivipara) carniolica (Squamata: Lacertidae) reflect the conditions of its selected microhabitat? // Salamandra. 2017. V. 53. № 1. P. 153–159.

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2. Fig. 1. An adult specimen of Darevskia valentini in its natural habitat (a) and the appearance of the skin of a juvenile D. valentini (b), on the left – dorsal side, on the right – ventral side, the red dashed line indicates the places where histology samples were taken (sagittal sections). The scale is 2 mm.

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3. Fig. 2. Microstructure of tubercular dorsal scales in adult specimens of Darevskia armeniaca (a), D. nairensis (b) and D. dahli (c) on sagittal sections: 1 – scale, 2 – Oberhäutchen – cuticle and β-layer, 3 – epidermis, 4 – melanophore layer, 5– dermis, 6 – lacuna of subcutaneous tissue, 7 – a blood vessel with erythrocytes, 8 – subcutaneous tissue, 9 – striated musculature, 10 – the cavity of the interstitial pocket. The arrows indicate osteoderms. Here and in Figures 3-6, a skin section at the resting stage of the epidermis. Staining with hematoclinin-eosin. Microphoto. The scale is 20 microns.

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4. Fig. 3. Microstructure of the abdominal shields of an adult Darevskia dahli on sagittal sections. A longitudinal skin fold on the ventral surface of the scales, forming an open tube (a). General view (b, d). Lacunae of subcutaneous tissue lying under the dermal layer (c). Designations as in Fig. 2, 11 – an open cavity of the tubular fold. Staining with hematoxylin-eosin. Microphoto. The scale is 20 microns.

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5. Fig. 4. Microstructure of tubercular dorsal scales (c) and abdominal shields (a, b, d) of adult specimens of Darevskia nairensis (a, b) and D. raddei (c, d) on sagittal sections. Notation as in Fig. 2, 3, 12 – xanthophore layer, 13 – pigmented lining of the abdominal cavity. Staining with hematoxylin-eosin + sudan W (lipid layers not detected) (c, d). Microphoto. The scale is 20 microns.

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6. Fig. 5. Microstructure of tubercular dorsal scales (a) and abdominal shields (b, c, d) of juvenile specimens of Darevskia valentini on sagittal sections: a, b – No. 7, c – No. 6, d – No. 5. The designations as in Fig. 2, 3, 4, 13 are a fat cell with a nucleus (indicated by an arrow). Staining with hematoxylin-eosin. Microphoto. The scale is 20 microns.

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7. Fig. 6. Microstructure of tubercular dorsal scales (a, b) and abdominal shields (c, d) of the trunk in an adult female Zootoca vivipara on sagittal sections. The designations as in Fig. 2-5, 14 are the skin fold. The arrow indicates the osteoderm. Staining with hematoclinin-eosin. Microphoto. The scale is 20 microns.

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8. Fig. 7. Diagram of the structure of the ventral scales of adult (a) and juvenile (b) lizards of the genus Darevskia: 1 – the cuticle (Oberhäutchen), 2 – the underlying layers of the epidermis and dermis, 3 – subcutaneous tissue with bundles of muscle fibers, 4 – subcutaneous musculature, 5 – the cavity of the intercostal pocket, 6 – connective tissue-a woven valve capable of locking the cavity of the interchannel pocket, 7 – skin folds of the bottom part of the interchannel pocket, 8 – skin diverticulum of the caudal edge of the flap.

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9. 8. The absolute thickness of the skin and its various layers (microns) on the dorsal (1) and ventral (2) parts of the body of the studied lizards. The thickness of the skin without a cuticle with a beta layer (a) (here are data on the thickness of the skin in both specimens of Zootoca vivipara), the thickness of the cuticle with a beta layer (b), and the epidermis (c).

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10. Fig. 9. The values of the thickness of the skin and its various layers (microns/mm) on the dorsal (1) and ventral (2) sides of the trunk of the studied lizards, reduced to body length (SVL). The total thickness of the skin (a), the thickness of the cuticle with the beta layer (b), and the epidermis (c).

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11. 10. The thickness of the cuticle with the β-layer (Ob+β: upper part of the diagram) and the epidermis (ep: lower part of the diagram) relative to the thickness of the entire skin on the dorsal (1) and ventral (2) parts of the body of the studied lizards.

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