Paedomorphosis in the Ezo salamander (Hynobius retardatus) rediscovered after almost 90 years

Zoological Letters - Tập 7 - Trang 1-9 - 2021
Hisanori Okamiya1, Ryohei Sugime2, Chiharu Furusawa3, Yoshihiro Inoue2, Osamu Kishida1
1Field Science Center for Northern Biosphere, Hokkaido University, Takaoka, Japan
2Graduate School of Environmental Science, Hokkaido University, Takaoka, Japan
3Graduate School of Environmental Science, Hokkaido University, Sapporo, Japan

Tóm tắt

Although paedomorphosis is widespread across salamander families, only two species have ever been documented to exhibit paedomorphosis in Hynobiidae. One of these two exceptional species is Hynobius retardatus in which paedomorphosis was first reported in 1924, in specimens from Lake Kuttara in Hokkaido. This population became extinct after the last observation in 1932; since then, no paedomorphs of this species have been reported anywhere. Here, we report the rediscovery of paedomorphs of this species. Three paedomorph-like male salamanders were collected from a pond in the south Hokkaido in December 2020 and April 2021; in size, these specimens were similar to metamorphosed adults but they still displayed larval features such as external gills and a well-developed caudal fin. An artificial fertilization experiment demonstrated that they were sexually compatible with metamorphosed females, thus, confirming them to be paedomorphs. Future efforts to find additional paedomorphs in this and other populations are required to assess the prevalence of paedomorphosis in H. retardatus and to improve understanding of the ecology and evolution of paedomorphisis in Urodela.

Tài liệu tham khảo

Gould SJ. Ontogeny and phylogeny. Cambridge: Harvard University Press; 1977. Wakahara M. Heterochrony and neotenic salamanders: possible clues for understanding the animal development and evolution. Zool Sci. 1996;13:765–76. Denoël M, Joly P, Whiteman HH. Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev. 2005;80:663–71. Smith TB, Skúlason S. Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst. 1996;27:111–33. Denoël M, Joly P. Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata). Proc R Soc Lond B Biol Sci. 2000;267:1481–5. Bonett RM, Ledbetter NM, Hess AJ, Herrboldt MA, Denoël M. Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development. Dev Dyn. 2021;2021:1–16. Whiteman HH. Evolution of facultative paedomorphosis in salamanders. Q Rev Biol. 1994;69:205–21. Whiteman HH, Wissinger SA, Denoël M, Mecklin CJ, Gerlanc NM, Gutrich JJ. Larval growth in polyphenic salamanders: making the best of a bad lot. Oecologia. 2012;168:109–18. AmphibiaWeb. Information on amphibian biology and conservation. 2021. http://amphibiaweb.org/. Accessed 15 Oct 2021. Frost DR. Amphibian species of the world: an online reference. Version 6.1. New York: American Museum of Natural History; 2021. https://amphibiansoftheworld.amnh.org/. Accessed 15 Oct 2021 Sasaki M. On a Japanese salamander, in Lake Kuttarush, which propagates like the axolotl. J College Agriculture, Hokkaido Imperial University, Sapporo, Japan. 1924;15:1–36. Sasaki M, Nakamura H. Relation of endocrine system to neoteny and skin pigmentation in a salamander, Hynobius lichenatus Boulenger. Annot Zool Japan. 1937;16:81–97. Jiang JP, Jia J, Zhang M, Gao KQ. Osteology of Batrachuperus londongensis (Urodela, Hynobiidae): study of bony anatomy of a facultatively neotenic salamander from mount Emei, Sichuan Province. China PeerJ. 2018;6:e4517. Moriya T, Makino S. On the hynobiid salamander (Hynobius retardatus) and neoteny reproduction. Collect Breed. 1980;42:317–22 (in Japanese). Moriya T. The effect of temperature on the action of thyroid hormone and prolactin in larvae of the salamander Hynobius retardatus. Gen Comp Endocrinol. 1983;49:1–7. Matsui M. Amphibians and reptiles in and around Lake Biwa. In: Kawanabe H, Nishino M, Maehata M, editors. Lake Biwa: interactions between nature and people. London: Springer Nature; 2012. p. 123–8. Sato I. A monograph of tailed batrachians of Japan. Osaka: Nippon Shuppan-sha; 1943. (in Japanese) Iwasawa H, Yamashita K. Normal stages of development of a hynobiid salamander, Hynobius nigrescens Stejneger. Jpn J Herpetol. 1991;14:39–62 (in Japanese with English abstract). Nishikawa K, Matsui M, Tanabe S, Sato S. Morphological and allozymic variation in Hynobius boulengeri and H. stejnegeri (Amphibia: Urodela: Hynobiidae). Zool Sci. 2007;24:752–66. Okamiya H, Sugawara H, Nagano M, Poyarkov NA. An integrative taxonomic analysis reveals a new species of lotic Hynobius salamander from Japan. PeerJ. 2018;6:e5084. Jömann N, Clemen G, Greven H. Notes on cranial ontogeny and delayed metamorphosis in the hynobiid salamander Ranodon sibiricus Kessler, 1866 (Urodela). Ann Anat. 2005;187:305–21. Makino S. Cytological observations on the fertilization of the egg of Hynobius retardatus Dunn. Jpn J Genet. 1935;10:223–33 (in Japanese). Kuramoto M. Further studies on sperm morphology of Japanese salamanders, with special reference to geographic and individual variation in sperm size. Jpn J Herpetol. 1997;17:1–10. Denoël M. Paedomorphosis in the Alpine newt (Triturus alpestris): decoupling behavioural and morphological change. Behav Ecol Sociobiol. 2002;52:394–9. Denoël M, Drapeau L, Winandy L. Reproductive fitness consequences of progenesis: sex-specific pay-offs in safe and risky environments. J Evol Biol. 2019;32:629–37. Wells KD. The ecology and behavior of amphibians. Chicago: University of Chicago Press; 2007.