Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques
Corresponding Author
David Glenn Smith
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
California National Primate Research Center, University of California–Davis, Davis, California
Department of Anthropology, University of California-Davis, One Shields Avenue, Davis, CA 95616Search for more papers by this authorJohn W. Mcdonough
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
Search for more papers by this authorDebra A. George
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
Search for more papers by this authorCorresponding Author
David Glenn Smith
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
California National Primate Research Center, University of California–Davis, Davis, California
Department of Anthropology, University of California-Davis, One Shields Avenue, Davis, CA 95616Search for more papers by this authorJohn W. Mcdonough
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
Search for more papers by this authorDebra A. George
Molecular Anthropology Laboratory, Department of Anthropology, University of California–Davis, Davis, California
Search for more papers by this authorAbstract
An 835 base pair (bp) fragment of mitochondrial DNA (mtDNA) was sequenced to characterize genetic variation within and among 1,053 samples comprising five regional populations each of longtail macaques (Macaca fascicularis) and rhesus macaques (Macaca mulatta), and one sample each of Japanese (M. fuscata) and Taiwanese (M. cyclopis) macaques. The mtDNA haplotypes of longtail macaques clustered in two large highly structured clades (Fas1 and Fas2) of a neighbor-joining tree that were reciprocally monophyletic with respect to those representing rhesus macaques, Japanese macaques, and Taiwanese macaques. Both clades exhibited haplotypes of Indonesian and Malaysian longtail macaques widely dispersed throughout them; however, longtail macaques from Indochina, Philippines, and Mauritius each clustered in a separate well-defined clade together with one or a few Malaysian and/or Indonesian longtail macaques, suggesting origins on the Sunda shelf. Longtail macaques from Malaysia and Indonesia were far more genetically diverse, and those from Mauritius were far less diverse than any other population studied. Nucleotide diversity between mtDNA sequences of longtail macaques from different geographic regions is, in some cases, greater than that between Indian and Chinese rhesus macaques. Approximately equal amounts of genetic diversity are due to differences among animals in the same regional population, different regional populations, and different species. A greater proportion of genetic variance was explained by interspecies differences when Japanese and Taiwanese macaques were regarded as regional populations of rhesus macaques than when they were treated as separate species. Rhesus macaques from China were more closely related to both Taiwanese and Japanese macaques than to their own conspecifics from India. Am. J. Primatol. 69:1–17, 2007. © 2006 Wiley-Liss, Inc.
REFERENCES
- Abegg C, Thierry B. 2002. Macaca evolution and dispersal in insular south-east Asia. Biol J Linn Soc 75: 555–576.
- Arnason U, Gullberg A, Burquete AS, Janke A. 2000. Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Hereditas 133: 217–228.
- Atkins H, Preston J, Cronk CB. 2001. A molecular test of Huxley's line: Cyrtandra (Gesneriaceae) in Borneo and the Philippines. Biol J Linn Soc 72: 143–159.
- Barker G, Barton H, Beavitt P, Bird M, Daly P, Doherty C, Gilbertson D, Hunt C, Krigbaum J, Lewis H, Manser J, McLaren S, Paz V, Piper P, Pyatt B, Rabett R, Reynolds T, Rose J, Rushworth G, Stephens M. 2002. Prehistoric foragers and farmers in southeast Asia: renewed investigations at Niah Cave, Sarawak. Proc Prehist Soc 68: 147–164.
10.1017/S0079497X00001481 Google Scholar
- Brandon-Jones D. 1996. The asian Colobinae (Mammalia: Cercopithecidae) as indicators of quarternary climate change. Biol J Linn Soc 59: 327–350.
- Brandon-Jones D. 1998. Pre-glacial Bornean primate impoverishment and Wallace's line. In: R Hall, JD Holloway, editors. Biogeography and geological evolution of SE Asia. Leiden, The Netherlands: Backhuys Publishers. p 393–404.
- Corbet GB, Hill JE. 1992. The mammals of the Indomalayan region: a systematic review. Oxford: Oxford University Press. 496p.
- Deinard A, Smith DG. 2001. Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. J Hum Evol 41: 45–59.
- Delson E. 1980. Fossil macaques, phyletic relationships and a scenario of deployment. In: DG Lindburg, editor. The macaques. Studies in ecology, behavior and evolution. New York: van Nostrand Rheinhold. p 10–30.
- Esselstyn JA, Widmann P, Heaney LR. 2004. The mammals of Palawan Island, Philippines. Proc Biol Soc Wash 117: 271–302.
- Eudey AA. 1980. Pleistocene glacial phenomena and the evolution of Asian macaques. In: DG Lindburg, editor. The macaques. Studies in ecology, behavior, and evolution. New York: van Nostrand Rheinhold. p 52–83.
- Excoffier L, Smouse P, Quatro J. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial restriction data. Genetics 131: 479–491.
- Felsenstein J. 2004. PHYLIP (Phylogeny Inference Package) version 3.6b. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
- Fooden J. 1976. Provisional classification and key to living species of macaques (Primates: Macaca). Folia Primatol 25: 225–236.
- Fooden J, Albrecht GH. 1993. Latitudinal and insular variation of skull size in crab-eating macaques. Am J Phys Anthropol 92: 521–538.
- Fooden J. 1995. Systematic review of southeast Asian longtail macaques, Macaca fascicularis (Raffles [1821]). Fieldiana Zool 81: 1–206.
- Fooden J, Albrecht GH. 1999. Tail length evolution in fascicularis-group macaques. Intern J Primatol 20: 431–440.
- Fooden J. 2000. Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Chicago: Field Museum of Natural History Fieldiana. 180p.
10.5962/bhl.title.7192 Google Scholar
- Groves C. 2001. Primate taxonomy. Washington: Smithsonian Institution Press. 350p.
- Hall R. 1996. Reconstructing Cenozoic SE Asia. In: R Hall, D Blundell, editors. Tectonic evolution of southeast Asia. London: Geological Society of London. p 153–184.
10.1144/GSL.SP.1996.106.01.11 Google Scholar
- Harihara S, Aota N, Hirai M, Terao, K, Cho F, Honjo S, Omota K. 1986. Polymorphism in the mitochondrial DNA of cynomolgous monkeys. Primates 27: 357–361.
- Harihara S, Saitou N, Hirai M, Aoto N, Terao K, Cho F, Honjo S, Omota K. 1988. Differentiation of mitochondrial DNA types in Macaca fascicularis. Primates 29: 117–127.
- Hayasaka K, Horai S, Shotake T, Nozawa K, Matsunaga E. 1986. Mitochondrial DNA polymorphism in Japanese monkeys, Macaca fuscata. Jpn J Genet 61: 345–359.
- Hayasaka K, Kawamoto Y, Shotake T, Nozawa K. 1987. Population genetical study of Japanese macaques, Macaca fuscata, in the Shimokita A1 troop, with special reference to genetic variability and relationships to Japanese macaques in other troops. Primates 28: 507–516.
- Hayasaka K, Horai S, Gojobori T, Shotake T, Nozawa K, Matsunaga E. 1988. Phylogenetic relationships among Japanese, rhesus, Formosan and crab-eating monkeys, inferred from restriction-enzyme analysis of mitochondrial DNAs. Mol Biol Evol 5: 270–281.
- 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: 1044–1053.
- Heaney LR. 1986. Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biol J Linn Soc 28: 127–165.
- Iwamoto M. 1975. On a skull of a fossil macaque from the Shikimizu limestone quarry in the Shikoku District, Japan. Primates 16: 83–94.
10.1007/BF02381801 Google Scholar
- Kamei T. 1969. Mammals of the glacial age in Japan–especially on Japanese monkey [in Japanese]. Monkey 106: 5–12.
- Kyes R, Jones-Engel L, Chalise MK, Engel G, Heidrich J, Grant R, Bajimaya SS, McDonough J, Smith DG, Ferguson B. 2006. Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal. Am J Primatol 68: 445–455.
- Joag SV, Stephens EB, Adams RJ, Foresman L, Narayan O. 1994. Pathogenesis of SIVMAC infection in Chinese and Indian rhesus macaques: effects of splenectomy on virus burden. J Virol 200: 436–446.
- Kondo M, Kawamoto Y, Nozawa K, Matsubayashi K, Watanabe T, Griffiths O, Stanley MA. 1993. Population genetics of crab-eating macaques (Macaca fascicularis) on the island of Mauritius. Am J Primatol 29: 167–182.
- Lawler SH, Sussman RW, Taylor LL. 1995. The mitochondrial DNA of the Mauritian macaques (Macaca fascicularis): an example of founder effect. Am J Phys Anthropol 96: 133–141.
- Ling B, Veazey RS, Luckay A, Penedo C, Xu K, Lifson JD, Marx P. 2002. SIVmac pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS 16: 1489–1496.
- Luzi P, Rafi MA, Victoria T, Baskin GB, Wenger DA. 1997. Characterization of the rhesus monkey galactocerebrosidase (GALC) cDNA and gene and identification of the mutation causing globoid cell leukodystrophy (Krabbe disease) in this primate. Genomics 42: 319–324.
- Marmi J, Bertranpetit J, Terradas J, Takenaka O, Domingo-Roura X. 2004. Radiation and phylogeography in the Japanese macaca, Macaca fuscata. Mol Phylogenet Evol 30: 676–685.
- Melnick DJ, Hoelzer GA, Absher R, Ashley MV. 1993. mtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol Biol Evol 10: 282–295.
- Morales JC, Melnick DJ. 1998. Phylogenetic relationships of the macaques. J Hum Evol 34: 1–23.
- Pusey AE, Packer C. 1987. Dispersal and philopatry. In: BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, TT Struhsaker, editors. Primate societies. Chicago: University of Chicago Press. p 250–266.
- Rosenblum LA, Supriatna J, Melnick DJ. 1997. Phylogeographic analysis of pigtail macaque populations (Macaca nemistrina) inferred from mitochondrial DNA. Am J Phys Anthropol 104: 35–46.
10.1002/(SICI)1096-8644(199709)104:1<35::AID-AJPA3>3.0.CO;2-C CAS PubMed Web of Science® Google Scholar
- Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
- Schneider S, Roessli D, Excofflier L. 2000. ARLEQUIN 2.001: a software for population genetic data analysis. Laboratory of Genetics and Biometry, University of Geneva, Switzerland.
- Smith DG. 2005. Genetic characterization of Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). Comp Med 55: 227–230.
- Smith DG, McDonough JW. 2005. Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am J Primatol 65: 1–25.
- Smith DG, George DA, McDonough JW. Genetic tests to identify the country of origin of and admixture between Indian and Chinese rhesus macaques (Macaca mulatta). Int J Primatol (in press).
- Sussman RW, Tattersall I. 1981. Behavior and ecology of Macaca fascicularis in Mauritius: a preliminary study. Primates 22: 192–205.
10.1007/BF02382610 Google Scholar
- Sussman RW, Tattersall I. 1986. Distribution, abundance and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern Indian Ocean. Folia Primatol 46: 28–43.
- Tosi AJ, Morales JC, Melnick DJ. 2000. Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Mol Phyl Evol 17: 133–144.
- Tosi AJ, Morales JC, Melnick DJ. 2002. Analysis of Macaca fascicularis Y-chromosome and mitochondrial markers indicate introgression with Indonesian rhesus and a biogeographic barrier in the Isthmus of Kra. Int J Primatol 23: 161–178.
- Tosi AJ, Morales JC, Melnick DJ. 2003. Paternal, maternal and bilateral molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution 57: 1419–1435.
- Voris HK. 2000. Maps of Pleistocene sea levels in southeast Asia: shorelines, river systems and time durations. J Biogeog 27: 1153–1167.
- Wallace AR. 1876. The geographical distribution of animals. London: Macmillan.
- Weiss ML, Goodman M, Prychodko W, Moore GW, Tanaka T. 1973. An analysis of macaque systematics using gene frequency data. J Hum Evol 2: 213–226.
- Woodruff DS. 2003. Neogene marine transgressions, paleogeography and biogeographic transitions on the Thai-Malay Peninsula. J Biogeogr 30: 551–567.
- Zhang Y-P, Shi LM. 1993. Phylogenetic relationships of macaques as inferred from restriction endonuclease analysis of mtDNA. Folia Primatol 60: 7–17.
