Advertisement

Mammalian Biology

, Volume 77, Issue 2, pp 113–123 | Cite as

Reevaluation of several taxa of Chinese lagomorphs (Mammalia: Lagomorpha) described on the basis of pelage phenotype variation

  • Deyan Ge
  • Andrey A. Lissovsky
  • Lin Xia
  • Cheng Cheng
  • Andrew T. Smith
  • Qisen YangEmail author
Original Investigation
First Online:

Abstract

Melanism is a common phenomenon in the animal kingdom. While the occurrence of melanism in lago-morphs has been less studied, this phenomenon has led to systematic confusion among different forms of pikas (Ochotona) and hares (Lepus). Within Ochotona, the Pianma black pika (O. nigritia) was established primarily based on its pelage phenotype variation compared with the sympatric Forrest’s pika (O. forresti). The Gaoligong pika (O. gaoligongensis) was also described based on pelage color differences with O. forresti. However, the specific status of these two taxa has been questioned for several years. We conducted a detailed examination of the cranial characters used for the initial diagnosis of each of these forms (O. forresti, O. gaoligongensis and O. nigritia). Insignificant differences were displayed among these species, thus contradicting the classification of O. gaoligongensis and O. nigritia asseparate species. Within Lepus, the Manchurian black hare (Lepus melainus) was also initially described based on the melanistic pelage possessed by this form. We conducted a detailed examination of the cranial characteristics of L. melainus and the sympatric Manchurian hare (L. mandshuricus) and confirmed the synonomy of these forms; L. melainus represents melanistic individuals of L. mandshuricus. These taxonomic mistakes probably resulted from underestimating the prevalence of melanism and the potential for adaptative variation of pelage coloration in nature. A more detailed study on the genetic background leading to the occurrence of melanistic lagomorphs is needed.

Keywords

Lagomorpha Lepus mandshuricus L. melainus Melanism Morphometric analysis Ochotona forresti O. gaoligongensis O. nigritia 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldous, C.M., 1939. A melanistic snowshoe hare from Maine. J. Hered. 30, 25–26.CrossRefGoogle Scholar
  2. Allen, G.M., 1938. The mammals of china and mongolia. Am. Mus. Nat. Hist., New York.Google Scholar
  3. Alves, P.C., Melo-Ferreira, J., Freitas, H., Boursot, P., 2008. The ubiquitous mountain hare mitochondria: multiple introgressive hybridization in hares, genus Lepus. Philos. Trans. R. Soc. B 363, 2831–2839.CrossRefGoogle Scholar
  4. Anderson, T.M., vonHoldt, B.M., Candille, S.I., Musiani, M., Greco, C., Stahler, D.R., Smith, D.W., Padhukasahasram, B., Randi, E., Leonard, J.A., et al., 2009. Molecular and evolutionary history of melanism in North American gray wolves. Science 323, 1339–1343.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Animal Diversity Web, 2011. Ochotona curzoniae (black-lipped pika). URL: https://doi.org/animaldiversity.ummz.umich.edu/site/resources/davidblank/leucisticpika.jpg/view.html (accessed 31.08.2011).
  6. Baccus, J.T., Posey, J.C., 1999. Melanism in white-tailed deer in central Texas. Southwest Nat. 44, 184–192.Google Scholar
  7. Belk, M.C., Smith, M.H., 1996. Pelage coloration in oldfield mice (Peromyscus poliono-tus): antipredator adaptation? J. Mammal. 77, 882–890.CrossRefGoogle Scholar
  8. Benson, S.B., 1933. Concealing coloration among some desert rodents of the southwestern United States. Univ. Cal. Publ. Zool. 40, 1–70.Google Scholar
  9. Blair, W.F., 1936. The Florida marsh rabbit. J. Mammal. 17, 197–207.CrossRefGoogle Scholar
  10. Bookstein, F.L., 1991. Morphometric Tools for Landmark Data: Geometry and Geology. Cambridge University Press, Cambridge.Google Scholar
  11. Chen, X., Li, W., 2009. A new subspecies of Ochotona forresti in southeastern Tibet, China. Acta Theriol. Sin. 29, 100–105 (in Chinese, English abstract).Google Scholar
  12. Corbet, G.B., 1978. The Mammals of the Palearctic Region: A Taxonomic Review. British Museum (Natural History), London.Google Scholar
  13. Ellerman, J.R., Morrison-Scott, T.C.S., 1951. Checklist of Palearctic and Indian Mammals 1758–1946. British Museum (Natural History), London.Google Scholar
  14. Eversmann, E., 1842. Addendaad Celeberrimi Pallassii Zoographiam Ross-Asiatican. Fasciculus 3. Izdatel’stovo Kazanskogo Universita, Kazan’, p. 19.Google Scholar
  15. Feng, Z.J., Kao, Y., 1974. Taxonomic notes on the Tibetan pika and allied species – including a new subspecies. Acta Zool. Sin. 20, 76–87 (in Chinese).Google Scholar
  16. Feng, Z.J., Zheng, C.L., 1985. Studies on the pikas (genus: Ochotona) of China - taxo-nomic notes and distribution. Acta Theriol. Sin. 5, 269–289 (in Chinese, English abstract).Google Scholar
  17. Feng, Z.J., Cai, G.Q., Zheng, C.L., 1986. The Mammals of Xizang. Science Press, Beijing (in Chinese).Google Scholar
  18. Flux, J.E.C., Angermann, R., 1990. The hares and jackrabbits. In: Chapman, J.A., Flux, J.E.C. (Eds.), Rabbits, Hares and Pikas, Status Survey and Conservation Action Plan. IUCN, Gland, Switzerland, pp. 61–110.Google Scholar
  19. Gong, Z.D., Wang, Y.X., Li, Z.H., Li, S.Q., 2000. A new species of pika: Pianma blacked Pika, Ochotona nigritia (Lagomorpha: Ochotonidae) from Yunnan. China Zool. Res. 21, 204–209 (in Chinese, English abstract).Google Scholar
  20. Gordon, D.C., 1954. Melanism in the varying hare, Lepus americanus virginianus. J. Mammal. 35, 122–122.CrossRefGoogle Scholar
  21. Gureev, A.A., 1964. Fauna of the USSR, mammals, vol. 3, part 10. Lagomorpha/Nauka, Moscow-Leningrad, in Russian.Google Scholar
  22. Hafner, D.J., Smith, A.T., 2010. Revision of the subspecies of the American pika, Ochotona princeps (Lagomorpha: Ochotonidae). J. Mammal. 91, 401–417.CrossRefGoogle Scholar
  23. Hoffmann, R.S., Smith, A.T., 2005. Order Lagomorpha. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference., 3rd ed. The Johns Hopkins University Press, Baltimore, pp. 185–211.Google Scholar
  24. Krupa, J.J., Geluso, K.N., 2000. Matching the color of excavated soil: cryptic coloration in the plains pocket gopher (Geomys bursarius). J. Mammal. 81, 86–96.CrossRefGoogle Scholar
  25. Lai, Y.C., Shiroishi, T., Moriwaki, K., Motokawa, M., Yu, H.T., 2008. Variation of coat color in house mice throughout Asia. J. Zool. (London) 274, 270–276.CrossRefGoogle Scholar
  26. Li, Z.Y., Luo, Z.X., 1979. On a new species of wild hare from China. J. North For. Univ. 2, 71–81 (in Chinese).Google Scholar
  27. Lu, X., 2003. Postnatal growth of skull linear measurements of Cape hare Lepus capen-sis in northern China: an analysis in an adaptive context. Biol. J. Linn. Soc. 78, 343–353.CrossRefGoogle Scholar
  28. Luo, Z.X., 1988. The Chinese Hare. China Forestry Publication House, Beijing, in Chinese.Google Scholar
  29. Majerus, M.E., Mundy, N.I., 2003. Mammalian melanism: natural selection in black and white. Trends Genet. 19, 585–588.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Marin, Y.F., 1984. Materials on the ecology of Altai pika in Telesk part of Altai preserve. In: Mlekopitayu-shchie Zapovednykh Territorii, Moscow, pp. 71–79 (in Russian).Google Scholar
  31. Nachman, M.W., Hoekstra, H.E., D’Agostino, S.L., 2003. The genetic basis of adaptive melanism in pocket mice. PNAS 100, 5268–5273.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Nakayama, K., Shotake, T., Takeneka, O., Ishida, T., 2008. Variation of the melanocortin 1 receptor gene in the macaques. Am. J. Primatol. 70, 778–785.PubMedCrossRefGoogle Scholar
  33. Niu, Y.D., Wei, F.W., Li, M., Liu, X.M., Feng, Z.J., 2004. Phylogeny ofpikas (Lagomorpha, Ochotona) inferred from mitochondrial cytochrome b sequences. Folia Zool. 53, 141–155.Google Scholar
  34. Ognev, S.I., 1922. Material on the systematics of the Russians hares. Ezhegodn. Zool. Muzeya Akad. Nauk 23, 485–491 (in Russian).Google Scholar
  35. Ognev, S.I., 1940. Mammals of the USSR and Adjacent Countries, vol. 4. Izdatel’stvo AN SSSR, Moscow, Leningrad, USSR, pp. 1–616, in Russian. English translation: Ognev, S.I., 1966. Mammals of the USSR and Adjacent Countries: Rodents. Israel Program for Scientific Translations, Jerusalem 4: 1–429.Google Scholar
  36. Pan, Q.H., Wang, Y.X., Yan, K., 2007. A Field Guide to the Mammals of China. China Forestry Publishing House, Beijing, in Chinese.Google Scholar
  37. Payseur, B.A., 2009. Y not introgress? Insights into the genetics of speciation in European rabbits. Mol. Ecol. 18, 23–24.PubMedPubMedCentralGoogle Scholar
  38. Radde, G., 1861. New mammal species from eastern Siberia. Bull. de l’ Acad. Imp. de St. Petersburg 3, 684–686 (in German).Google Scholar
  39. Robinson, R., 1978. Homologous coat color variation in Felis. Carnivore (Seattle) 1, 68–71.Google Scholar
  40. Robinson, T.J., Elder, F.F., Chapman, J.A., 1983. Karyotypic conservatism in the genus Lepus (order Lagomorpha). Can. J. Genet. Cytol. 25, 540–544.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Rohlf, F.J., 2003. tpsRelw, relative warps analysis, version 1.36. Department of Ecology and Evolution, State University of New York at Stony Brook.Google Scholar
  42. Rohlf, F.J., 2005. tpsDig, digitize landmarks and outlines, version 2.05. Department of Ecology and Evolution, State University of New York at Stony Brook.Google Scholar
  43. Rohlf, F.J., Slice, D.E., 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39, 40–59.CrossRefGoogle Scholar
  44. Searle, A.G., 1968. Comparative Genetics of Coat Colour in Mammals. Logos Press, London.Google Scholar
  45. Sheets, H.D., 2003. IMP-Integrated Morphometrics Package. Department of Physics, Canisius College, Buffalo, New York.Google Scholar
  46. Sludskiy, A.A., Bernschtein, A.D., Schubin, I.G., Fadeev, V.A., Orlov, G.I., Bai-tanaev, O.A., bekenov, A., Kapitonov, V.I., Utinov, S.R., 1980. Mammals of Kazakhstan, vol. 2. Lagomorpha, Nauka, Kazakh SSR, Alma-Ata, Kazakhstan (in Russian).Google Scholar
  47. Smith, A.T., Formozov, A.N., Hoffmann, R.S., Zheng, C.L., Erbajeva, M.A., 1990. The pikas. In: Chapman, J.A., Flux, J.E.C. (Eds.), Rabbits, Hares and Pikas, Status Survey and Conservation Action Plan. IUCN, Gland, Switzerland, pp. 14–60.Google Scholar
  48. Smith, A.T., Johnston, C.H., 2011a. Ochotona nigritia. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.1. www.iucnredlist.org. (Accessed 31.08.2011).Google Scholar
  49. Smith, A.T., Johnston, C.H., 2011b. Ochotona gaoligongensis. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.1. www.iucnredlist.org. (Accessed 31.08.2011).Google Scholar
  50. Smith, A.T., Johnston, C.H., 2011c. Ochotona forresti. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.1. www.iucnredlist.org. (Accessed 31.08.2011).Google Scholar
  51. Smith, A.T., Weston, M.L., 1990. Ochotona princeps. Mammal. Spec. 352, 1–8.CrossRefGoogle Scholar
  52. Smith, A.T., Xie, Y., 2008. A Guide to the Mammals of China. Princeton University Press, Princeton.Google Scholar
  53. Sokolov, V.E., Ivanitskaya, E.Y., Gruzdev, V.V., Geptner, V.G., 1994. Mammals of Russia and Adjacent Regions. Lagomorpha, Nauka, Moscow, in Russian. English translation: Sokolov, V.E., Ivanitskaya, E.Y., Gruzdev, V.V., Geptner, V.G., 2009. Lagomorphs: Mammals of Russia and Adjacent Regions. Smith, A.T. (Scientific Ed.). Smithsonian Institution Libraries, Washington, DC.Google Scholar
  54. Sowerby, A.C., 1923. The Naturalist in Manchuria, vol. 2. Tientsin Press, Tientsin.Google Scholar
  55. Stoner, C.J., Bininda-Emonds, O.R.P., Caro, T., 2003. The adaptive significance of coloration in lagomorphs. Biol. J. Linn. Soc. 79, 309–328.CrossRefGoogle Scholar
  56. Thomas, O., 1923. On mammals from the Li-Kiang Range, Yunnan, being a further collection obtained by Mr. George Forrest. Ann. Mag. Nat. His. 11, 655–663.CrossRefGoogle Scholar
  57. Velich, R., 1956. Mammals from eastern Nebraska. J. Mammal. 37, 271–272.CrossRefGoogle Scholar
  58. Wang, Y.X., Gong, Z.D., Duan, X.D., 1988. A new species of Ochotona (Ochotonidae, Lagomorpha) from Mt. Gaoligong, northwest Yunnan. Zool. Res. 9, 201–207 (in Chinese).Google Scholar
  59. Weston, M.L., 1982. Anumerical revision of the genus Ochotona (Lagomorpha:Mam-malia) and an examination of its phylogenetic relationships. Ph.D. dissertation, University of British Columbia, Vancouver.Google Scholar
  60. Wu, C.H., Wu, J.P., Bunch, T.D., Li, Q.W., Wang, Y.X., Zhang, Y.P., 2005. Molecular phylogenetics and biogeography of Lepus in eastern Asia basedonmitochondrial DNA sequences. Mol. Phylogenet. Evol. 37, 45–61.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Ye, J., Nie, W., Wang, J., Su, W., Jing, M., Graphodatsky, A.S., Yang, F., 2011. Genome-wide comparative chromosome map between human and the Forrest’s pika (Ochotona forresti) established by cross-species chromosome painting: further support for the Glires hypothesis. Cytogenet. Genome Res. 132, 41–46.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Yu, N., Zheng, C., Feng, Z., 1992. The phylogenetic analysis of subgenus Ochotona of China. Acta Theriol. Sin. 12, 255–266 (in Chinese, English abstract).Google Scholar
  63. Yudakov, A.G., Nikolaev, L.G., 1974. Some Data on the Biology of Caprolagus (Allo-lagus) brachyurus mandschuricus Radde, vol. 17. Trudy biol.-pochvenn. Inst., Vladivostok, pp. 65–74, in Russian.Google Scholar
  64. Zhang, R.Z., 1997. Distribution of Mammalian Species in China. Chinese Forestry Publishing House, Beijing, in Chinese.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • Deyan Ge
    • 1
  • Andrey A. Lissovsky
    • 2
  • Lin Xia
    • 1
  • Cheng Cheng
    • 3
  • Andrew T. Smith
    • 4
  • Qisen Yang
    • 1
    Email author
  1. 1.Key Laboratory of Zoological Systematics and EvolutionInstitute of Zoology, Chinese Academy of SciencesBeijingChina
  2. 2.Zoological MuseumMoscow State UniversityMoscowRussia
  3. 3.Biology DepartmentChina West Normal UniversitySichuanChina
  4. 4.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations

Cite article

Buy options