Primates

, Volume 47, Issue 2, pp 158–164 | Cite as

Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island

Original Article

Abstract

The Japanese macaques (Macaca fuscata yakui) on Yakushima Island are an endemic subspecies and are closely related to the population of Kyushu, one of the main islands of Japan. Using feces collected throughout Yakushima Island, we examined mitochondrial DNA (mtDNA) to investigate the phylogeography of Japanese macaques. Six haplotypes were observed for a 203-bp fragment of the mtDNA control region. The nucleotide diversity (π) was low (0.0021). The genetic divergence within the Yakushima population was lower (0.009) than that among four haplotypes of the Kyushu population (0.015), calculated using Kimura’s two-parameter method. The mismatch distribution analysis of the six haplotypes of the Yakushima population suggested that the Yakushima population had experienced a sudden expansion in population size, which could be related to the bottleneck effect. The geographic distribution of the mtDNA haplotypes was not uniform. One haplotype was distributed widely, whereas the other five haplotypes were distributed only in the lowlands. The low genetic diversity and biased distribution are discussed in relation to an environmental crash caused by ancient volcanic activity near this island, which is postulated to have happened about 7,300 years ago, and the delayed recovery of highland vegetation.

Keywords

Bottleneck Low genetic diversity Macaca fuscata yakui MtDNA Phylogeography 

References

  1. Avise JC, Arnold J, Ball RM, Berminghame E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography—the mitochondrial-DNA bridge between population-genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  2. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  3. Eguchi T (1984) Climate of Yaku-shima Island, especially regionality of precipitation distribution. In: Nature Conservation Bureau, Environment Agency, Japan (eds) Conservation reports of the Yaku-shima wilderness area, (in Japanese with English summary). Kyushu, Japan, pp 3–26Google Scholar
  4. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327CrossRefPubMedGoogle Scholar
  5. Fukuzawa H (1995) Non-glacial varved lake sediment as a natural timekeeper and detector on environmental changes (in Japanese with English abstract). Quat Res 34:135–149Google Scholar
  6. Geographical Survey Institute, Japan (2004) http://www.gsi.go.jp/
  7. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715–6719PubMedGoogle Scholar
  8. Goodman SJ, Tamate HB, Wilson R, Nagata J, Tatsuzawa S, Swanson GM, Pemberton JM, Mccullough DR (2001) Bottlenecks, drift and differentiation: the population structure and demographic history of sika deer (Cervus nippon) in the Japanese archipelago. Mol Ecol 10:1357–1370CrossRefPubMedGoogle Scholar
  9. Hanya G, Yoshihiro S, Zamma K, Matsubara H, Ohtake M, Kubo R, Noma N, Agetsuma N, Takahata Y (2004) Environmental determinants of the altitudinal variations in relative group densities of the Japanese macaques on Yakushima. Ecol Res 19:485–493CrossRefGoogle Scholar
  10. Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66: 591–600PubMedGoogle Scholar
  11. Hayaishi S, Kawamoto Y (2002) Fecal genotyping of mitochondrial DNA polymorphism and fecal age-class estimation of Macaca fuscata yakui: a preliminary report (in Japanese with English abstract). Honyurui Kagaku 42:161–166Google Scholar
  12. Hayasaka K, Ishida T, Horai S (1991) Heteroplasmy and polymorphism in the major non-coding region of mitochondrial DNA in Japanese monkeys: association with tandemly repeated sequences. Mol Biol Evol 8:399–415PubMedGoogle Scholar
  13. Itani J (1972) Social structure of primates (in Japanese). Kyoritsu Shuppan, TokyoGoogle Scholar
  14. Iwamoto M, Hasegawa Y (1972) Two macaque fossil teeth from the Japanese Pleistocene. Primates 13:77–81CrossRefGoogle Scholar
  15. Japan Meteorological Agency (2004) http://www.jma.go.jp/
  16. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405. DOI 10.1016/S0968-0004(98)01285-7CrossRefPubMedGoogle Scholar
  17. Kan YW, Dozy AM, Trecartin R, Todd D (1977) Identification of a nondeletion defect in α-thalassemia. N Engl J Med 297:1081–1084PubMedGoogle Scholar
  18. Kawamura Y (1994) Late Pleistocene to Holocene mammalian faunal succession in the Japanese islands, with comments on the late Quaternary extinctions. Archaeozoologia 6:7–22Google Scholar
  19. Kawamoto Y (1999) Origin of Japanese macaques in views from genes (in Japanese). Kagaku 69:300–305Google Scholar
  20. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  21. Kimura M (2000) Paleogeography of the Ryukyu Islands. Tropics 10:5–24Google Scholar
  22. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245CrossRefPubMedGoogle Scholar
  23. Kurose N, Kaneko Y, Abramov AV, Siriaroonrat B, Masuda R (2001) Low genetic diversity in Japanese population of the Eurasian badger Meles meles (Mustelidae, Carnivora) revealed by mitochondrial cytochrome b gene sequences. Zool Sci 18:1145–1151CrossRefGoogle Scholar
  24. Machida H, Arai F (1978) Akahoya Ash-A Holocene widespread tephra erupted from the Kikai Caldera, south Kyushu, Japan (in Japanese with English abstract). Quat Res 17:143–163Google Scholar
  25. Machida H, Arai F (1992) Atlas of tephra in and around Japan (in Japanese). University of Tokyo Press, TokyoGoogle Scholar
  26. Matsuhashi T, Masuda R, Mano T, Yoshida MC (1999) Microevolution of the mitochondrial DNA control region in the Japanese brown bear (Ursus arctos) population. Mol Biol Evol 16:676–684PubMedGoogle Scholar
  27. Mouri T, Agatsuma T, Iwagami M, Kawamoto Y (2000) Species identification by mitochondrial DNA: a case study of macaque remains from Shuri Castle, Okinawa (in Japanese with English abstract). Primate Research 16:87–94Google Scholar
  28. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  29. Nozawa K, Shotake T, Ohkura Y, Tanabe Y (1977) Genetic variations within and between species of Asian macaques. Jpn J Genet 52:15–30Google Scholar
  30. Nozawa K, Shotake T, Kawamoto Y, Tanabe Y (1982) Population genetics of Japanese monkeys: II. Blood protein polymorphisms and population structure. Primates 23:252–271Google Scholar
  31. Nozawa K, Shotake T, Minezawa M, Kawamoto Y, Hayasaka K, Kawamoto S, Ito S (1991) Population genetics of Japanese monkeys: III Ancestry and differentiation of local populations. Primates 32:411–435Google Scholar
  32. Oi T (1988) Sociological study on the troop fission of wild Japanese monkeys (Macaca fuscata yakui) on Yakushima Island. Primates 29:1–19Google Scholar
  33. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  34. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615Google Scholar
  35. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  36. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Department of Anthropology, University of GenevaGoogle Scholar
  37. Shigesada N, Kawasaki K, Teramoto E (1986) Traveling periodic waves in heterogeneous environments. Theor Popul Biol 30:143–160CrossRefGoogle Scholar
  38. Shotake T, Ohkura Y, Nozawa K (1975) A fixed state of the PGM-2mac allele in the population of the Yaku macaque (Macaca fuscata yakui). In: Contemporary Primatology, 5th International Congress on Primates, Nagoya 1974. Karger, Basel, pp 67–74Google Scholar
  39. Sprague DS, Suzuki S, Takahashi H, Sato S (1998) Male life history in natural populations of Japanese macaques: migration, dominance rank, and troop participation of males in two habitats. Primates 39:351–363Google Scholar
  40. Tomaru N, Mitsutsuji T, Takahashi M, Tsumura Y, Uchida K, Ohba K (1997) Genetic diversity in Fagus crenata (Japanese beech): influence of the distributional shift during the late-Quaternary. Heredity 78:241–251CrossRefGoogle Scholar
  41. Tukada M (1982) Cryptomeria japonica: glacial refugia and late-glacial and postglacial migration. Ecology 63:1091–1105Google Scholar
  42. Uehara S (1975) The importance of the temperate forest elements among woody food plants utilized by Japanese monkeys and its possible historical meaning for the establishment of the monkeys’ range—a preliminary report. In: Contemporary Primatology, 5th International Congress on Primates, Nagoya 1974. Karger, Basel, pp 392–400Google Scholar
  43. Ui T (1973) Exceptionally far-reaching, thin pyroclastic flow in southern Kyushu, Japan (in Japanese with English abstract). Bull Volc Soc Jpn, Second Ser 18:153–168Google Scholar
  44. White OL, Densmore III LD (1992) Mitochondrial DNA isolation. In: Hoelzel AR (eds) Molecular genetic analysis of populations, a practical approach, 1st edn. IRL Press, Oxford, pp 29–55Google Scholar
  45. Yamagiwa J, Hill DA (1998) Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. Primates 39:257–273Google Scholar
  46. Yoshihiro S, Furuichi T, Manda M, Ohkubo N, Kinoshita M, Agetsuma N, Azuma S, Matsubara H, Sugiura H, Hill D, Kido E, Kubo R, Matsushima K, Nakajima K, Maruhashi T, Oi T, Sprague D, Tanaka T, Tsukahara T, Takahata Y (1998) The distribution of wild Yakushima macaque (Macaca fuscata yakui) troops around the coast of Yakushima Island, Japan. Primate Research 14:179–187Google Scholar
  47. Yoshihiro S, Ohtake M, Matsubara H, Zamma K, Hanya G, Tanimura Y, Kubota H, Kubo R, Arakane T, Hirata T, Furukawa M, Sato A, Takahata Y (1999) Vertical distribution of wild Japanese macaques (Macaca fuscata yakui) in the western area of Yakushima Island, Japan: preliminary report. Primates 40:409–415Google Scholar

Copyright information

© Japan Monkey Centre and Springer-Verlag 2006

Authors and Affiliations

  1. 1.Laboratory of Human Evolution Studies, Graduate School of ScienceKyoto UniversitySakyo, KyotoJapan
  2. 2.Population Genetics Section, Primate Research InstituteKyoto UniversityInuyamaJapan

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