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Mammalian Biology

, Volume 69, Issue 1, pp 28–45 | Cite as

Phylogenetic relationships between Indian and Burmese hares (Lepus nigricollis and L. peguensis) inferred from epigenetic dental characters

  • F. SuchentrunkEmail author
Original investigation

Abstract

Systematic relationships among several forms of hares from South and Southeast Asia currently included in the Indian hare, Lepus nigricollis, and the Burmese hare, L peguensis, are not well understood. In this study, 29 epigenetic occlusal characters (enamel fold patterns) were analyzed quantitatively to infer phylogenetic relationships among the following operational taxonomie units (0TU): L. n. nigricollis (n = 29), L. n. singhala (n = 9), L. n. simcoxi (n = 18), L n. mahadeva (n = 7), L. n. dayanus (n = 29), L. n. ruficaudatus (n = 52), and L. peguensis (L. p. peguensis, L p. siamensis, L p. vassali, combined n = 25). Pairwise epigenetic distances (C. A. B. Smith’s MMD) among OTUs were calculated from OTU-specific frequencies of character states. All cluster analyses performed on the distance matrices revealed close relationships among the OTUs of L. nigricollis, including rufous-tailed hares, L. n. ruficaudatus, and an only slightly separate status of Burmese hares, but a distinct separation of both Indian and Burmese hares from woolly hares, L. oiostolus (n = 27), and Chinese hares, L. sinensis (n = 28), that where used as outgroups. The results conformed the current provisional systematic evaluation, positioning rufous-tailed hares within Indian hares, but rendering the separate species status of L. peguensis still open.

Keywords

Lepus Indian hare Burmese hare teeth meristic characters 

Phylogenetische Beziehungen zwischen indischen Hasen und burmesischen Hasen (Lepus nigricollis und L. peguensis) anhand epigenetischer Zahnmerkmale

Zusammenfassung

Die Hasen (Genus Lepus) des süd- und südostasiatischen Festlandes werden - abgesehen von L. ca-pensis, L. comus, L. oiostolus und L. sinensis - provisorisch zu zwei Arten zusammengefaßt; zu den indischen Hasen (L. nigricollis) und den burmesischen Hasen (L. peguensis). Innerhalb der ersteren Art werden provisorisch 13 und innerhalb der letzteren Art drei Subspecies unterschieden. Einzelne Formen von L. nigricollis könnten eigene Arten darstellen, zu L. peguensis oder auch zu L. capensis gehören. L. nigricollis und L. peguensis könnten auch Vertreter einer Art sein. Quantitative morpho-logische Analysen fehlen, urn die einzelnen Hypothesen zu stützen. In dieser Untersuchung wurden die Frequenzen von 29 non-metrischen Merkmalen der Zahnoberflächen indischer und burmesischer Hasen zur Berechnung “epigenetischer Distanzen” (C.A.B: Smith’s MMD - “Mean Measure of Divergence”) zwischen folgenden “operationalen taxonomischen Einheiten” (OTU) herangezogen: L. n. dayanus (n = 29), L. n. mahadeva (n = 7), L. n. nigricollis (n = 29), L. n. simcoxi (n = 18), L. n. singhala (n = 9), L. n. ruficaudatus (n = 52), und L. peguensis (n = 25). Verschiedene Cluster-Analysen der paarweisen MMD-Werte ergaben unter Einbeziehung von L. oiostolus (n = 27) und L. sinensis (n = 28) eine sehr enge Beziehung zwischen den OTUs von L. nigricollis und L. peguensis. Dies spricht für die Zugehörigkeit aLLer untersuchter OTUs zu L. nigricollis und stützt die Ansicht, daß. L. nigricollis und L. peguensis konspezifisch seien.

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References

  1. Alves, P. C.; Ferrand, N.; Suchentrunk, F. (2001): Developmental stability and protein heterozygosity in a local population of Iberian hares (Lepus granatensis). Mamm. biol. 66, 238–250.Google Scholar
  2. Alves, P. C.; Ferrand, N.; Suchentrunk, E.; Harris, D. J. (2003): Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula. Mol. Phylogenet. Evol., in press.Google Scholar
  3. Anscombe, E. J. (1948): The transformation of Poisson, binomial and negative-binomial data. Biometrika 35, 246–254.CrossRefGoogle Scholar
  4. Angermann, R. (1965): Revision der palaeark-tischen und äthiopischen Arten der Gattung Lepus (Leporidae, Lagomorpha). Diss. Thesis, Humboldt University of Berlin.Google Scholar
  5. Angermann, R. (1966): Beiträge zur Kenntnis der Gattung Lepus (Lagomorpha, Leporidae). I. Abrenzung der Gattung Lepus. Mitt. Zool. Mus., Berlin 42, 127–144.Google Scholar
  6. Angermann, R. (1967): Beitrag zur Kenntnis der Gattung Lepus (Lagomorpha, Leporidae) IV. Lepus yarkandensis Gunther, 1875 und Lepus oiostolus Hodgson, 1840 - zwei endemische Hasenarten Zentralasiens. Mitt. Zool. Mus. Berlin 43, 189–203.CrossRefGoogle Scholar
  7. Angermann, R. (1983): The taxononmy of Old World Lepus. Acta Zool. Fennica 174, 17–21.Google Scholar
  8. Angermann, R.; Feiler, A. (1988): Zur Nomen-klatur, Artabgrenzung und Variabilitát der Hasen (Gattung Lepus) im westlichen Afrika (Mammalia, Lagomorpha, Leporidae). Zool. Abh. Staat. Mus. Tierkd. Dresden 43, 149–167.Google Scholar
  9. Bergmans, W. (1995): On mammals from the People’s Democratic Republic of Laos, mainly from Sekong Province and Hongsa Special Zone. Z. Säugetierkunde 60, 286–306.Google Scholar
  10. Berry, R. J. (1963): Epigenetic polymorphism in wild populations of Mus musculus. Genet. Res. Camb. 4, 193–220.CrossRefGoogle Scholar
  11. Blanford, W. T (1891): The fauna of British India, including Ceylon and Burma. London: Taylor and Francis.Google Scholar
  12. Blanford, W. T (1901): The distribution of vertebrate animals in India, Ceylon, and Burma. Phil. Trans. Roy. Soc. Lond. B 194, 335–436.CrossRefGoogle Scholar
  13. Chakraborty, S. (1983): Records of the Zoological Society of India: Contributions to the mammalian fauna of Jammu and Kashmir, India. Calcutta: Director of Zool. Soc. of India, Miscell. Publ. Occas. Paper 38.Google Scholar
  14. Corbet, G. B.; Hill, J. E. (1992): The mammals of the Indomalayan Region: A systematic review. Oxford: Oxford Univ. Press.Google Scholar
  15. Ellerman, J. R.; Morrison-Scott, T. C. S. (1951): Checklist of Palearctic and Indian mammals. London: British Museum.Google Scholar
  16. Erbaeva, M. A.; Angermann, R. (1983): Das Originalmaterial von Serengetilagus praecapensis DIETRICH, 1941 - ergänzende Beschreibung und vergleichende Diskussion. Schrif-tenr. geol. Wiss., Berlin 19/20, 39–60.Google Scholar
  17. Felsenstein, J. (1985). Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle Scholar
  18. Flux, J. E. C. (1983): Introduction to taxonomic problems in hares. Acta Zool. Fennica 174, 7–10.Google Scholar
  19. Flux, I.E.; Flux, M. M. (1983): Taxonomy and distribution of East African hares. Acta Zool. Fennica 174, 41–43.Google Scholar
  20. Flux, J. E. C.; Angermann, R. (1990): Hares and Jackrabbits. In: Rabbits, Hares and Pikas. Status Survey and Conservation Action Plan. Ed. by J. A. Chapman and J. E. C. Flux. Gland: IUCN/SSC Lagomorph Specialist Group. Pp. 61–94.Google Scholar
  21. Forsyth Major, C. I. (1898): On fossil and recent Lagomorpha. Trans. Lin. Soc. Lond. 7, 433–520.CrossRefGoogle Scholar
  22. Ghose, R. K. (1967): Notes on the taxonomy and distribution of the Pachmarhi hare, Lepus ni-gricollis mahadeva Wroughton and Ryley [Mammalia: Lagomorpha: Leporidae]. J. Bombay Nat. Hist. Soc. 64, 355–358.Google Scholar
  23. Ghose, R. K. (1971): Field observations on the habits of the Pachmarhi Hare, Lepus nigricol-lis mahadeva Wroughton and Ryley, in Madhya Pradesh, India. J. Zool. Soc. India 23, 167–169.Google Scholar
  24. Ghose, R. K. (1978): Observations on the ecology and status of the Hispid hare in Rajagarh Forest, Darrang District, Assam, in 1975 and 1976. J. Bombay Nat. Hist. Soc. 75, 206–209.Google Scholar
  25. Ghose, R. K. (1981): On the ecology and status of the hispid hare. In: Proc. World Lagomorph Conference, August 12–16, 1979. Ed. by K. Myers and C. D. Mcinnes. Gland: IUCN Pp. 918–925.Google Scholar
  26. Ghose, R. K.; Ghosal, D. K. (1984): Recent occurrence of the Hispid hare, Caprolagus hispi-dus (Pearson), in the Duars of West Bengal. Bull. zool. Surv. India 6, 315–316.Google Scholar
  27. Glover, M. A. (1938): The Mammals of China and Mongolia. New York: The American Museum of Natural History.Google Scholar
  28. Grassman, L. I. Jr. (2000): Movements and diet of the leopard cat Prioailurus bengalensis in a seasonal evergreen forest in south-central Thailand. Acta Theriol. 45, 421–426.CrossRefGoogle Scholar
  29. Grüneberg, H. (1965): Genes and genotypes affecting the teeth of the mouse. J. Embryol. Exp. Morph. 14, 137–159.PubMedPubMedCentralGoogle Scholar
  30. Hibbard, C. W. (1963): The origin of the P3 pattern of Sylvilagus, Caprolagus, Oryctolagus and Lepus. J. Mammalogy 44, 1–15.CrossRefGoogle Scholar
  31. Jayson, E. A. (1999): Habiat preferences of five herbivores in the Chimmony Wildlife Sanctuary. Indian Forester 125, 975–985.Google Scholar
  32. Jerdan, T. C. (1984): A handbook of the mammals of India. A Natural History of all the animals known to inhabit Indian Subcontinent. Delhi: Mittal Publications.Google Scholar
  33. Jerdon, T. C. (1867): The Mammals of India. Natural history of all the animals known to inhabit continental India. Roorkee: Thomason College Press.CrossRefGoogle Scholar
  34. Jerdon, T. C. (1874): The Mammals of India; A natural History of all the Animals known to inhabit continental India. London: J. Wheldon.CrossRefGoogle Scholar
  35. Lande, R. (1981): The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99, 541–543.PubMedPubMedCentralGoogle Scholar
  36. Lekagul, B.; Mcneely, J. A. (1977): Mammals of Thailand. Bangkok: Kurusapha Ladprao Press.Google Scholar
  37. Lord Medway (1978): The Wild Mammals of Malaya and Offshore Islands including Singapore. Kuala Lumpur: Oxford Univ. Press.Google Scholar
  38. Lydekker, R. (1900): The Great and Small Game of India, Burma, and Tibet. London: Rowland Ward Ltd.Google Scholar
  39. Lynch, M.; Walsh, B. (1998): Genetics and Analysis of Quantitative Traits. Sunderland: Sinauer Assoc, Inc.Google Scholar
  40. Manakadan, R.; Rahmani, A. R. (1999): Population densities of the blacknaped hare Lepus nigricollis nigricollis at Rollapadu Wildlife Sanctuary, Kurnool district, Andhra Pradesh. J. Bombay Nat. Hist. Soc. 96, 221–224.Google Scholar
  41. Miller, W. E.; Carranza-Cataneda, O. (1982): New lagomorphs from the Pliocene of central Mexico. J. Vertebr. Paleont. 2, 95–107.CrossRefGoogle Scholar
  42. Møller, A. P.; Swaddle, J. P. (1997): Asymmetry, Developmental Stability, and Evolution. Oxford: Oxford Univ. Press.Google Scholar
  43. Nowak, R. M. (Ed.) (1999): Walker’s Mammals of the World. 5th ed. Vol I. Baltimore, London: John Hopkins Press.Google Scholar
  44. Ossenberg, N. (1981): An argument for the use of total side frequencies of bilateral nonmetric skeletal traits in population distance analysis: The regression of symmetry on incidence. Am. J. Phys. Anthropol. 54, 471–479.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Palacios, F. A. (1996): Systematics of the indigenious hares of Italy traditionally identified as Lepus europaeus Pallas, 1778 (Mammalia: Leporidae). Bonner Zool. Beitr. 46, 59–61.Google Scholar
  46. Palacios, F. A.; Lopez, N.M. (1980): Morphología dentaria de las liebres europeas (Lagomorpha, Leporidae). Doñana, Acta Vertebr. 7, 61–81.Google Scholar
  47. Palmer, A. R.; Strobeck, C. (1986): Fluctuating asymmetry: measurement, analysis, patterns. Ann. Rev. Ecol. Syst. 17, 391–421.CrossRefGoogle Scholar
  48. Petter, F. (1959): Eléments d’une révision des lièvre africains du sous-genre Lepus. Mammalia 23, 41–67.Google Scholar
  49. Petter, F. (1961): Eléments d’une révision des Lievres européens et asiatiques du sous-genre Lepus. Z. Säugetierkunde 26, 30–40.Google Scholar
  50. Phillips, W. W. A. (1981): Manual of the Mammals of Sri Lanka. Part II. 2nd rev. ed. Colombo: Wildlife and Nature Protection Society of Sri Lanka.Google Scholar
  51. Prater, S. H. (1980): The Book of Indian Mammals. 4th ed. Bombay: Bombay Nat. Hist. Soc.Google Scholar
  52. Rice, W. S. (1989): Analyzing tables of statistical tests. Evolution 43, 223–225.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Roberts, T. J. (1977): The Mammals of Pakistan. London and Tonbridge: Ernest Benn Ltd.Google Scholar
  54. Robinson, T. J. (1986): Incisor morphology as an aid in the systematics of the South African Leporidae (Mammalia: Lagomorpha). S. Afr. J. Zool. 21, 297–302.Google Scholar
  55. Schnell, G. D.; Selander, R. K. (1981): Environmental and morphological correlates of genetic variation in mammals. In: Mammalian Population Genetics. Ed. by M. H. Smith and J. Joule. Athens: Univ. Georgia Press. Pp. 60–99.Google Scholar
  56. Sclater, W. L. (1891): Catalogue of Mammalia in the Indian Museum, Calcutta. Part II. Calcutta: Governm. of India, Central Printing Office.Google Scholar
  57. Shrestha, T. K. (1997): Mammals of Nepal. Kathmandu: Mrs. Bimala Shrestha.Google Scholar
  58. Siddiqi, M. S. U (1969): Fauna of Pakistan. Karachi: Agric. Res. Council, Government of Pakistan.Google Scholar
  59. Sjøvold, T. (1977): Non-metrical divergence between skeletal populations. Ossa 4 (Suppl. 1), 1–133.Google Scholar
  60. Sody, H. J. V (1939): Lepus nigricollis, de Zwartnek-Haas. De Tropische Natuur 28, 161–168.Google Scholar
  61. Sterndale, R. A. (1884): Natural History of the Mammalia of India and Ceylon. Calcutta: Thacker, Spink and Co.Google Scholar
  62. Suchentrunk, F. (1993): Variability of minor tooth traits and allozymic diversity in brown hare Lepus europaeus populations. Acta Theriol., Suppl. 2, 59–69.CrossRefGoogle Scholar
  63. Suchentrunk, F. (2000): Epigenetic dental asymmetry of Israeli hares: developmental stability along an environmental gradient. Israel J. Zool. 46, 103–118.CrossRefGoogle Scholar
  64. Suchentrunk, E.; Flux, J. E.C. (1996): Minor dental characters in East African cape hares and savanna hares (Lepus capensis and Lepus victoriae): A study of intra- and interspecific variability. J. Zool. (London) 238, 495–511.CrossRefGoogle Scholar
  65. Suchentrunk, E.; Willing, R.; Hartl, G. (1991): On eye lens weights and other age criteria of the Brown hare (Lepus europaeus Pallas, 1778). Z. Säugetierkunde 56, 365–374.Google Scholar
  66. Suchentrunk, E.; Willing, R.; Hartl, G. B. (1994): Non-metrical polymorphism of the first lower premolar (P3) in Austrian brown hares (Lepus europaeus): a study on regional differentiation. J. Zool. (London) 232, 79–91.CrossRefGoogle Scholar
  67. Suchentrunk, E.; Alkon, P. U.; Willing, R.; Yomtov, Y. (2000): Epigenetic dental variability of Israeli hares (Lepus sp.): ecogenetic or phylogenetic causation? J. Zool. (London) 252, 503–515.CrossRefGoogle Scholar
  68. Tate, G. H. H. (1947): Mammals of Eastern Asia. New York: The Macmillan Comp.CrossRefGoogle Scholar
  69. Tiwari, K. K.; Ghose, R. K.; Chakraborty, S. (1971): Notes on a collection of small mammals from Western Ghats, with remarks on the status of Rattus rufescens (Gray) and Bandicota indica malabarica (Shaw). J. Bombay Nat. Hist. Soc. 68, 378–384.Google Scholar
  70. Thorpe, R. S.; Brown, R. P.; Malhotra, A.; Wuster, W. (1991): Geographic variation and population systematics: distinguishing between ecogenetics and phylogenetics. Boll. Zool. 58, 329–335.CrossRefGoogle Scholar
  71. Thulin, C.-G.; Tegelström, H. (2002): Biased geographical distribution of mitochondrial DNA that passed the species barrier from mountain hares to brown hares (genus Lepus): an effect of genetic incompatibility and mating behaviour? J. Zool. (London) 258, 299–306.CrossRefGoogle Scholar
  72. VAN Peenen, P. E D.; Ryan, P. E.; Light, R. H. (1969): Preliminary Identification Manual for Mammals of South Vietnam. Washington DC: U.S. National Mus. Smithsonian Institution.Google Scholar
  73. Wilson, D. E.; Reeder, D A. M. (Eds.) (1993): Mammal Species of the World - A Taxonomic and Geographic Reference. 2nd ed. Washington, London: Smithsonian Inst. Press.Google Scholar
  74. Wroughton, R. C. (1915): Bombay Natural History Socienty’s mammal survey of India, Burma and Ceylon. Report No. 16. J. Bombay Nat. Hist. Soc. 23, 460–480.Google Scholar
  75. Wroughton, R. C. (1921): Summary of the Indian Mammal Survey of the Bombay Natural History Society - part VI. Family I. - Leporidae. J. Bombay Nat. Hist. Soc. 27, 66–70.Google Scholar
  76. Zhang, Y.; Jin, S.; Quan, G.; Li, S.; Ye, Z.; Wang, E.; Zhang, M. (1997): Distribution of mammalian species in China. Beijing: China Forestry Publishing House.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2004

Authors and Affiliations

  1. 1.Research Institute of Wildlife EcologyUniversity of Veterinary MedicineViennaViennaAustria

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