Primates

, Volume 53, Issue 4, pp 397–411 | Cite as

Variability of tail length in hybrids of the Japanese macaque (Macaca fuscata) and the Taiwanese macaque (Macaca cyclopis)

  • Yuzuru Hamada
  • Ayumi Yamamoto
  • Yutaka Kunimatsu
  • Sayaka Tojima
  • Toshio Mouri
  • Yoshi Kawamoto
Original Article

Abstract

In primates, tail length is subject to wide variation, and the tail may even be absent. Tail length varies greatly between each species group of the genus Macaca, which is explained by climatic factors and/or phylogeographic history. Here, tail length variability was studied in hybrids of the Japanese (M. fuscata) and Taiwanese (Macaca cyclopis) macaque, with various degrees of hybridization being evaluated through autosomal allele typing. Relative tail length (percent of crown–rump length) correlated well with the number of caudal vertebrae. Length profiles of caudal vertebrae of hybrids and parent species revealed a common pattern: the length of several proximal-most vertebrae do not differ greatly; then from the third or fourth vertebra, the length rapidly increases and peaks at around the fifth to seventh vertebra; then the length plateaus for several vertebrae and finally shows a gentle decrease. As the number of caudal vertebrae and relative tail length increase, peak vertebral length and lengths of proximal vertebrae also increase, except that of the first vertebra, which only shows a slight increase. Peak vertebral length and the number of caudal vertebrae explained 92 % of the variance in the relative tail length of hybrids. Relative tail length correlated considerably well with the degree of hybridization, with no significant deviation from the regression line being observed. Thus, neither significant heterosis nor hybrid depression occurred.

Keywords

Macaca fuscata Macaca cyclopis Hybridization Tail Caudal vertebrae Japanese macaque Taiwanese macaque 

References

  1. Abegg C (2006) The role of contingency in the evolution of the Barbary macaque. In: Hodges JK, Cortes J (eds) The Barbary macaque: biology, management and conservation. Nottingham Univ Press, Nottingham, pp 17–27Google Scholar
  2. Ackermann RR, Rogers J, Cheverud J (2006) Identifying the morphological signatures of hybridization in primate and human evolution. J Hum Evol 51:632–645PubMedCrossRefGoogle Scholar
  3. Aimi M (1994) Numerical Variation of Vertebrae in Japanese Macaques, Macaca fuscata. Anthropol Sci 102(Suppl):1–10Google Scholar
  4. Ankel F (1962) Vergleichende Untersuchungen uber die Skelettmorphologie des Greifschwanzes Sudamerikanischer Affen (Platyrrhina). Z Morph Okol Tiere 52:131–170CrossRefGoogle Scholar
  5. Ankel F (1965) Der Canalis Sacralis als Indikator fur die Lange der Caudalregion der Primaten. Folia Primatol (Basel) 3:263–276CrossRefGoogle Scholar
  6. Ankel F (1972) Vertebral morphology of fossil and extant primates. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago, pp 223–240Google Scholar
  7. Biswas J, Borah DK, Das J, Bhattacharjee PC, Mohnot SM, Horwich RH (2011) The enigmatic Arunachal Macaque: its biogeography, biology and taxonomy in Northeastern India. Am J Primatol 73:458–473PubMedCrossRefGoogle Scholar
  8. Bonhomme M, Cuartero S, Blancher A, Crouan-Roy B (2008) Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis). J Heredity 100:158–169CrossRefGoogle Scholar
  9. Chakraborty D, Ramakrishnan U, Panor J, Mishra C, Sinha A (2007) Phylogenetic relationships and morphometric affinities of the Arunachal macaque Macaca munzala, a newly described primate from Arunachal Pradesh, northeastern India. Mol Phylogenet Evol 44:838–849PubMedCrossRefGoogle Scholar
  10. Deinard A, Smith DG (2001) Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. J Hum Evol 41:45–59PubMedCrossRefGoogle Scholar
  11. Delson E (1980) Fossil macaques, phyletic relationships and scenario of deployment. In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold, New York, pp 10–29Google Scholar
  12. Eudey AA (1980) Pleistocene glacial phenomena and the evolution of Asian macaques. In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold, New York, pp 52–83Google Scholar
  13. Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic Press, San Diego, p 596Google Scholar
  14. Fooden J (1964) Rhesus and Crab-Eating Macaques: intergradation in Thailand. Science 143:362–363CrossRefGoogle Scholar
  15. Fooden J (1967) Complementary specialization of male and female reproductive structures in the bear macaque (Macaca arctoides). Nature 214:939–941Google Scholar
  16. Fooden J (1975) Taxonomy and evolution of liontail and pigtail macaques (Primates: cercopithecidae). Fieldiana Zool 67:1–169Google Scholar
  17. Fooden J (1976) Provisional classification and key to living species of macaques (primates: Macaca). Folia Primatol (Basel) 25:225–236CrossRefGoogle Scholar
  18. Fooden J (1980) Classification and distribution of living macaques (Macaca Lacépède, 1799). In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold, New York, pp 1–9Google Scholar
  19. Fooden J (1982) Ecogeographic segregation of macaque species. Primates 23:574–579Google Scholar
  20. Fooden J (1988) Taxonomy and evolution of the sinica group of macaques: 6. Interspecific comparisons and synthesis. Fieldiana Zool 45:1–44Google Scholar
  21. Fooden J (1990) The bear macaque, Macaca arctoides: a systematic review. J Hum Evol 19:607–686Google Scholar
  22. Fooden J (1995) Systematic review of Southeast Asian longtail macaques, Macaca fascicularis (Raffles, [1821]). Fieldiana Zool 81:1–206Google Scholar
  23. Fooden J (1997) Tail length variation in Macaca fascicularis and M. mulatta. Primates 38(3):221–231CrossRefGoogle Scholar
  24. Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana Zool 96:1–180Google Scholar
  25. Fooden J (2001) Systematic review of Taiwanese macaques, Macaca cyclopis Swinhoe, 1863. Fieldiana Zool 98:1–70Google Scholar
  26. Fooden J, Albrecht GH (1999) Tail length variation in Fascicularis-group macaques (Cercopithecidae: Macaca). Int J Primatol 20(3):431–440CrossRefGoogle Scholar
  27. Gebo DL, Sargis EJ (1994) Terrestrial adaptations in the postcranial skeletons of guenons. Am J Phys Anthropol 93:341–371PubMedCrossRefGoogle Scholar
  28. German RZ (1982) The functional morphology of caudal vertebrae in new world monkeys. Am J Phys Anthropol 58:453–459PubMedCrossRefGoogle Scholar
  29. Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington, p 350Google Scholar
  30. Hamada Y (1994) Standard growth patterns and variations in growth patterns of the Japanese monkeys (Macaca fuscata) based on an analysis by the spline function method. Anthropol Sci 102(suppl.):57–76Google Scholar
  31. Hamada Y, Yamamoto A (2010) Morphological characteristics, growth, and aging in Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese Macaques. Springer, Tokyo, pp 27–52CrossRefGoogle Scholar
  32. Hamada Y, Hayakawa S, Suzuki J, Watanabe K, Ohkura S (2003) Seasonal variation in the body fat of Japanese macaques Macaca fuscata. Mammal Study 28:79–88CrossRefGoogle Scholar
  33. Hamada Y, Watanabe T, Chatani K, Hayakawa S, Iwamoto M (2005) Morphometrical comparison between Indian- and Chinese- derived rhesus macaques (Macaca mulatta). Anthropol Sci 113:183–188CrossRefGoogle Scholar
  34. Hamada Y, Urasopon N, Hadi I, Malaivijitnond S (2006) Body size and proportions and pelage color of free-ranging rhesus macaques (Macaca mulatta) from a zone of hybridization in Northeastern Thailand. Int J Primatol 27:497–513CrossRefGoogle Scholar
  35. Hamada Y, Suryobroto B, Goto S, Malaivijitnond S (2008) Are northern long-tailed macaques (Macaca fascicularis fascicularis) hybrids with southern rhesus macaques (M. mulatta)? Morphological and body color variation in Thai Macaca fascicularis fascicularis North and South of the Isthmus of Kra. Int J Primatol 29:1271–1294CrossRefGoogle Scholar
  36. Hamada Y, Kurita H, Goto S, Morimitsu Y, Malaivijitnond S, Pathonton S, Pathonton B, Kingsada P, Vongsombath C, Samouth F, Praxaysombath B (2010) Distribution and present status of macaques in Lao PDR. In: Nadler T, Rawson BM, Thinh VN (eds) Conservation of primates in Indochina. Frankfurt Zoological Society and Conservation International, Hanoi, pp 27–42Google Scholar
  37. Hayasaka K, Fujii K, Horai S (1996) Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA. Mol Biol Evol 13:1044–1053PubMedCrossRefGoogle Scholar
  38. Iwamoto M (1971) Morphological Studies of Macaca fuscata: VI. Somatometry. Primates 12:151–174CrossRefGoogle Scholar
  39. Iwamoto M, Hamada Y, Watanabe T (1984) Eruption of deciduous teeth in Japanese monkeys (Macaca fuscata). J Anthropol Soc Nippon 92:273–279 (in Japanese with English Abstract)CrossRefGoogle Scholar
  40. Iwamoto M, Watanabe T, Hamada Y (1987) Eruption of permanent teeth in Japanese monkeys (Macaca fuscata). Primate Res 3:18–28 (in Japanese with English Abstract)CrossRefGoogle Scholar
  41. Kawamoto Y (2005) NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan. Primates 46:203–206PubMedCrossRefGoogle Scholar
  42. Larson SG, Stern JT Jr (2006) Maintenance of above-branch balance during primate arboreal quadrupedalism: coordinated use of forearm rotators an tail motion. Am J Phys Anthropol 129:71–81Google Scholar
  43. Li DY, Xu HL, Smith DG, Chen AC, Trask JS, Zhu Q, Yao YF, Du DD, Ni QY (2011) Phylogenetic analysis of Chinese rhesus macaques (Macaca mulatta) based on mitochondrial control region sequence. Am J Primatol 73:883–895PubMedCrossRefGoogle Scholar
  44. Malaivijitnond S, Sae-Low W, Hamada Y (2008) The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand. J Med Primatol 37:31–37PubMedGoogle Scholar
  45. Nakatsukasa M, Ward CV, Walker A, Teaford MF, Kunimatsu Y, Ogihara N (2004) Tail loss in Proconsul heseloni. J Hum Evol 46:777–784Google Scholar
  46. Narita Y, Kuratani S (2005) Evolution of the vertebral formulae in mammals: a perspective on developmental constraints. J Exper Zool (Mol Dev Evol) 304B:91–106CrossRefGoogle Scholar
  47. Organ JM (2010) Structure and function of platyrrhine caudal vertebrae. Anat Rec 293:730–745CrossRefGoogle Scholar
  48. Organ JM, Lemelin P (2011) Tail architecture and function of Cebupithecia sarmientoi, a middle Miocene platyrrhine from La Venta, Colombia. Anat Rec 294:2013–2023CrossRefGoogle Scholar
  49. Osawa H, Morimitsu Y, Kawamoto Y, Muroyama Y, Maekawa S, Nigi H, Tori H, Goto S, Maruhashi T, Nakagawa N, Nakatani J, Tanaka T, Hayakawa S, Yamada A, Hayaishi S, Seino H, Saeki M, Kawai S, Hagiwara H, Suzuki K, Suzuki K, Uetsuki S, Okano M, Okumura T, Yoshida A, Yokoyama N (2005) Population explosion of Taiwanese macaques in Japan. Nat Hist J Chulalongkorn Univ Supple 1:55–60Google Scholar
  50. Roos C, Ziegler T, Hodges JK, Zischeler H, Abegg C (2003) Molecular Phylogeny of Mentawai macaques: taxonomic and biogeographic implication. Mol Phylogen Evol 29:139–150CrossRefGoogle Scholar
  51. Russo GA, Shapiro LJ (2011) Morphological correlates of tail length in the catarrhine sacrum. J Hum Evol 61:223–232PubMedCrossRefGoogle Scholar
  52. Schultz AH (1969) The life of primates. Weidenfeld and Nicolson, Hampshire, p 281Google Scholar
  53. Sinha A, Datta A, Madhusudan MD, Charudutt M (2005) The Arunachal macaque Macaca munzala: a new species from western Arunachal Pradesh, northeastern India. Int J Primatol 26:977–989CrossRefGoogle Scholar
  54. Sokrith H, Naven H (2010) A new record of Macaca fascicularis × M. mulatta hybrids in Cambodia. Cambodian J Nat Hist 1:7–11Google Scholar
  55. Tosi AJ, Morales JC, Melnick DJ (2002) Y-Chromosome and Mitochondrial Markers in Macaca fascicularis Indicate Introgression with Inodochinese M. mulatta and a Biogeographic Barrier in the Isthmus of Kra. Int J Primatol 23:161–178CrossRefGoogle Scholar
  56. Wilson DR (1972) Tail reduction in Macaca. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago, pp 241–261Google Scholar
  57. Wolpert L, Jessel T, Lawrence P, Meyerowitz E, Robertson E, Smith J (2007) Principles of development, 3rd edn. Oxford Univ Press, New York, p 551Google Scholar
  58. Ziegler T, Abegg C, Meijaard E, Perwitasari-Farajallah D, Walter L, Hodges JK, Roos C (2007) Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group. Mol Phylogenet Evol 42:807–816Google Scholar

Copyright information

© Japan Monkey Centre and Springer 2012

Authors and Affiliations

  • Yuzuru Hamada
    • 1
  • Ayumi Yamamoto
    • 2
  • Yutaka Kunimatsu
    • 3
  • Sayaka Tojima
    • 3
  • Toshio Mouri
    • 1
  • Yoshi Kawamoto
    • 4
  1. 1.Evolutionary Morphology Section, Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Nursing Course, School of MedicineGifu UniversityGifuJapan
  3. 3.Laboratory of Physical Anthropology, Department of Biology, Faculty of ScienceKyoto UniversityKyotoJapan
  4. 4.Genome Diversity Section, Primate Research InstituteKyoto UniversityInuyamaJapan

Personalised recommendations