Skip to main content

Advertisement

Log in

Hybridization and Stratification of Nuclear Genetic Variation in Macaca mulatta and M. fascicularis

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

We used genotypes for 13 short tandem repeats (STRs) to assess the genetic diversity within and differentiation among populations of rhesus macaques (Macaca mulatta) from mainland Asia and long-tailed macaques (M. fascicularis) from mainland and insular Southeast Asia. The subjects were either recently captured in the wild or derived from wild-caught founders maintained in captivity for biomedical research. A large number of alleles are shared between the 2 macaque species but a significant genetic division between them persists. The distinction is more clear-cut among populations that are not, or are unlikely to have recently been, geographically contiguous. Our results suggest there has been significant interspecific nuclear gene flow between rhesus macaques and long-tailed macaques on the mainland. Comparisons of mainland and island populations of long-tailed macaques reflect marked genetic subdivisions due to barriers to migration. Geographic isolation has restricted gene flow, allowing island populations to become subdivided and genetically differentiated. Indonesian long-tailed macaques show evidence of long-term separation and genetic isolation from the mainland populations, whereas long-tailed macaques from the Philippines and Mauritius both display evidence of founder effects and subsequent isolation, with the impact from genetic drift being more profound in the latter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abegg, C., & Thierry, B. (2002). Macaque evolution and dispersal in insular south-east Asia. Biological Journal of the Linnean Society. Linnean Society of London, 75, 555–576. doi:10.1046/j.1095-8312.2002.00045.x.

    Article  Google Scholar 

  • Ackermann, R. R., Rogers, J., & Cheverud, J. M. (2006). Identifying the morphological signatures of hybridization in primate and human evolution. Journal of Human Evolution, 51, 632–645. doi:10.1016/j.jhevol.2006.07.009.

    Article  PubMed  Google Scholar 

  • Allendorf, F. W. (1983). Isolation, gene flow and genetic differentiation among populations. In C. M. Shonewald-Cox, S. M. Chambers, B. MacBryde, & L. Thomas (Eds.), Genetics and Conservation (pp. 51–65). London: Benjamin-Cummings.

    Google Scholar 

  • Andrade, M. C. R., Penedo, M. C. T., Ward, T., Silva, V. F., Bertolini, L. R., Roberts, J. A., et al. (2004). Determination of genetic status in a closed colony of rhesus monkeys (Macaca mulatta). Primates, 45, 183–186. doi:10.1007/s10329-004-0084-x.

    Article  PubMed  Google Scholar 

  • Bonhomme, M., Blancher, A., Cuarteros, S., Chikhi, L., & Crouau-Roy, B. (2008). Origin and number of founders in an introduced insular primate: Estimation from nuclear genetic data. Molecular Ecology, 17, 1009–1019. doi:10.1111/j.1365-294X.2007.03645.x.

    Article  PubMed  CAS  Google Scholar 

  • Bynum, E. L., Bynum, D. Z., & Supriatna, J. (1997). Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in Central Sulawesi, Indonesia. American Journal of Primatology, 43, 181–209. doi:10.1002/(SICI)1098-2345(1997)43:3<181::AID-AJP1>3.0.CO;2-T.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, J. (2000). Vaccine studies stymied by shortage of animals. Science, 287, 959–960. doi:10.1126/science.287.5455.959.

    Article  PubMed  CAS  Google Scholar 

  • Delson, E. (1980). Fossil macaques, phyletic relationships and a scenario of deployment. In D. G. Lindburg (Ed.), The Macaques: Studies in ecology, behavior, and evolution (pp. 10–30). New York: Van Nostrand–Reinhold.

    Google Scholar 

  • Doxiadis, G. G. M., Otting, N., de Groot, N. G., de Groot, N., Rouweler, A. J. M., Noort, R., Vershoor, E. J., Bontjer, I., Bontrop, R. E. (2003). Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics, 55, 540–551.

    Article  PubMed  CAS  Google Scholar 

  • Doxiadis, G. G. M., Rouweler, A. J. M., de Groot, N. G., Louwerse, A., Otting, N., Verschoor, E. J., et al. (2006). Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques. Immunogenetics, 58, 259–268. doi:10.1007/s00251-006-0083-8.

    Article  PubMed  CAS  Google Scholar 

  • Evans, B. J., Supriatna, J., & Melnick, D. J. (2001). Hybridization and population genetics of two macaque species in Sulawesi, Indonesia. Evolution; International Journal of Organic Evolution, 55, 1685–1702.

    Google Scholar 

  • Ferguson, B., Street, S. I., Wright, H., Pearson, C., Jia, Y., Thompson, S. L., et al. (2007). Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics, 8, 43. doi:10.1186/1471-2164-8-43.

    Article  PubMed  Google Scholar 

  • Fittinghoff Jr, N. A., & Lindburg, D. G. (1980). Riverine refuging in east Bornean Macaca fascicularis. In D. G. Lindburg (Ed.), The Macaques: Studies in ecology, behavior and evolution. New York: Van Nostrand Reinhold.

    Google Scholar 

  • Fooden, J. (1964). Rhesus and crab-eating macaques: integradation in Thailand. Science, 143, 363–364.

    Article  PubMed  Google Scholar 

  • Fooden, J. (1976). Primates obtained in peninsular Thailand June-July, 1973, with notes on the distribution of continental Southeast Asian leaf-monkeys (Presbytis). Primates, 17, 95–118. doi:10.1007/BF02381570.

    Article  Google Scholar 

  • Fooden, J. (1995). Systematic review of Southeast Asian longtail macaques, Macaca fascicularis (Raffles 1821). Fieldiana Zoology, 81, 1–206.

    Google Scholar 

  • Fooden, J. (1997). Tail length variation in Macaca fascicularis and M. mulatta. Primates, 38, 221–232. doi:10.1007/BF02381611.

    Article  Google Scholar 

  • Fooden, J. (2000). Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Field Museum of Natural History, Chicago.

  • Froehlich, J., Supriatna, J., & Muskita, Y. (1996). Biodiversity and the conservation biology of Macaca nigra: An anthropological view. Tropical Biodiversity, 3, 85–102.

    Google Scholar 

  • Groves, C. P. (2001). Primate Taxonomy. Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Hamada, Y., Ohsawa, H., Urasopon, N., & Malaivijitnond, S. (2004). Preliminary report on the distribution and status of macaques in Thailand. Primate Report, 20, 97–108 in Japanese doi:10.2354/psj.20.97.

    Article  Google Scholar 

  • Hamada, Y., Urasopon, N., Hadi, I., & Malaivijitnond, S. (2006). Body size, proportions and pelage color of free-ranging rhesus macaques (Macaca mulatta) from a zone of hybridization in northern Thailand. International Journal of Primatology, 27, 497–513. doi:10.1007/s10764-006-9033-4.

    Article  Google Scholar 

  • Hayasaka, K., Fujii, K., & Horai, S. (1996). Molecular phylogeny of macaques: implications of nucleotide sequences from a 896-base pair region of mitochondrial DNA. Molecular Biology and Evolution, 13, 1044–1053.

    PubMed  CAS  Google Scholar 

  • Hernandez, R. D., Hubisz, M. J., Wheeler, D., Smith, D. G., Ferguson, B., Rogers, J., et al. (2007). Demographic histories and patterns of linkage disequilibrium for Chinese and Indian rhesus macaques. Science, 316, 240–243. doi:10.1126/science.1140462.

    Article  PubMed  CAS  Google Scholar 

  • Joag, S. V., Stephens, E. B., Adams, R. J., Foresman, L., & Narayan, O. (1994). Pathogenesis of SIVmac infection in Chinese and Indian rhesus macaques: Effects of splenectomy on virus burden. Virology, 200, 436–446. doi:10.1006/viro.1994.1207.

    Article  PubMed  CAS  Google Scholar 

  • Jombart, T. (2008). adegenet: An R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford, England), submitted.

  • Kanthaswamy, S., Gill, L., Satkoski, J., Goyal, V., Malladi, V., Kou, A., et al. The development of a Chinese-Indian hybrid (Chindian) rhesus macaque colony at the California National Primate Research Center (CNPRC) by introgression. Journal of Medical Primatology, in press.

  • Kanthaswamy, S., & Smith, D. G. (1998). Use of microsatellite polymorphisms for paternity exclusion in rhesus macaque (Macaca mulatta). Primates, 39, 135–145. doi:10.1007/BF02557726.

    Article  Google Scholar 

  • Kanthaswamy, S., & Smith, D. G. (2004). Effects of geographic origins on captive Macaca mulatta mtDNA variation. Journal of Comparative Medicine, 54, 166–174.

    Google Scholar 

  • Kanthaswamy, S., Von Dollen, A., Kurushima, J. D., Alminas, O., Rogers, J., Ferguson, B., et al. (2006). Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta). American Journal of Primatology, 68, 73–95. doi:10.1002/ajp.20207.

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto, Y., Ischak, T. M., & Supriatna, J. (1984). Genetic variations within and between troops of the crab-eating macaque (Macaca fascicularis) on Sumatra, Java, Bali, Lombok and Sumbawa, Indonesia. Primates, 25, 131–159. doi:10.1007/BF02382387.

    Article  Google Scholar 

  • Kawamoto, Y., Kawamoto, S., Matsubayashi, K., Nozawa, K., Watanabe, T., Stanley, M. A., et al. (2008). Genetic diversity of longtail macaques (Macaca fascicularis) on the island of Mauritius: An assessment of nuclear and mitochondrial DNA polymorphisms. Journal of Medical Primatology, 37, 45–54. doi:10.1111/j.1600-0684.2007.00225.x.

    PubMed  CAS  Google Scholar 

  • Krebs, K. C., Jin, Z., Rudersdorf, R., Hughes, A. L., & O’Connor, D. H. (2005). Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques. Journal of Immunology (Baltimore, MD.: 1950), 175, 5230–5239.

    CAS  Google Scholar 

  • Kyes, R., Jones-Engel, L., Chalise, M. K., Engel, G., Heidrich, J., Grant, R., et al. (2006). Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal. American Journal of Primatology, 68, 445–455. doi:10.1002/ajp.20240.

    Article  PubMed  CAS  Google Scholar 

  • Ling, B., Veazey, R. S., Luckay, A., Penedo, C., Xu, K., Lifson, J. D., et al. (2002). SIVmac pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS (London, England), 16, 1489–1496. doi:10.1097/00002030-200207260-00005.

    Google Scholar 

  • Malaivijitnond, S., Wattana, S. -L., & Yuzuru, H. (2008). The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand. Journal of Medical Primatology, 37, 31–37.

    PubMed  Google Scholar 

  • Malhi, R. S., Sickler, B., Lin, D., Satkoski, J., George, D., Kanthaswamy, S., et al. (2007). MamuSNP: A SNP resource for Rhesus macaques (Macaca mulatta). PLoS ONE, 2(5), e438. doi:10.1371/journal.pone.0000438.

    Article  PubMed  Google Scholar 

  • Marmi, J., Bertranpetit, J., Terradas, J., Takenaka, O., & Domingo-Roura, X. (2004). Radiation and phylogeography in the Japanese macaque, Macaca fuscata. Molecular Phylogenetics and Evolution, 30, 676–685. doi:10.1016/S1055-7903(03)00247-1.

    Article  PubMed  CAS  Google Scholar 

  • Melnick, D. J., Hoelzer, G. A., Absher, R., & Ashley, M. V. (1993). mtDNA diversity in rhesus monkey reveals overestimates of divergence time and paraphyly with neighboring species. Molecular Biology and Evolution, 10, 282–295.

    PubMed  CAS  Google Scholar 

  • Morales, J. C., & Melnick, D. J. (1998). Phylogenetic relationships of the macaques (Cercopithecidae: Macaca) as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. Journal of Human Evolution, 34, 1–23. doi:10.1006/jhev.1997.0171.

    Article  PubMed  CAS  Google Scholar 

  • Morin, P. A., Kanthaswamy, S., & Smith, D. G. (1997). Simple sequence repeat, SSR, polymorphisms for colony management and population genetics in rhesus macaques (Macaca mulatta). American Journal of Primatology, 42, 199–213. doi:10.1002/(SICI)1098-2345(1997)42:3<199::AID-AJP3>3.0.CO;2-S.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press: New York.

    Google Scholar 

  • Penedo, M. C. T., Bontrop, R. E., Heijmans, C. M. C., Offing, N., Noort, R., Rouweler, A. J. M., et al. (2005). Microsatellite typing of the rhesus macaque MHC region. Immunogenetics, 57, 198–209. doi:10.1007/s00251-005-0787-1.

    Article  PubMed  CAS  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    PubMed  CAS  Google Scholar 

  • Raymond, M., & Rousset, F. (1995). GENEPOP: Population genetics software for exact tests and ecumenicism. The Journal of Heredity, 86, 248–249.

    Google Scholar 

  • Satkoski, J., George, D., Smith, D. G., & Kanthaswamy, S. (2007). Genetic characterization of wild and captive rhesus macaques in China. Journal of Medical Primatology. www.blackwell-synergy.com/doi/abs/10.1111/j.1600-0684.2007.00228.x.

  • Slatkin, M. (1981). Estimating levels of gene flow in natural populations. Genetics, 99, 323–335.

    PubMed  Google Scholar 

  • Slatkin, M. (1985). Gene flow in natural populations. Annual Review of Ecology and Systematics, 16, 393–430. doi:10.1146/annurev.ecolsys.16.1.393.

    Article  Google Scholar 

  • Slatkin, M., & Barton, N. H. (1989). A comparison of three indirect methods for estimating the average level of gene flow. Evolution; International Journal of Organic Evolution, 43, 1349–1368. doi:10.2307/2409452.

    Google Scholar 

  • Smith, D. G., & McDonough, J. (2005). Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). American Journal of Primatology, 65, 1–25. doi:10.1002/ajp.20094.

    Article  PubMed  CAS  Google Scholar 

  • Smith, D. G., George, D., Kanthaswamy, S., & McDonough, J. (2006). Identification of country of origin and admixture between Indian and Chinese rhesus macaques. International Journal of Primatology, 27, 881–898. doi:10.1007/s10764-006-9026-3.

    Article  Google Scholar 

  • Smith, D. G., McDonough, J. W., & George, D. A. (2007). Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques. American Journal of Primatology, 69, 182–189. doi:10.1002/ajp.20337.

    Article  PubMed  CAS  Google Scholar 

  • Street, S. L., Kyes, R. C., Grant, R., & Ferguson, B. (2007). Single nucleotide polymorphisms (SNPs) are highly conserved in rhesus (Macaca mulatta) and cynomolgus (Macaca fascicularis) macaques. BMC Genomics, 8, 480. doi:10.1186/1471-2164-8-480.

    Article  PubMed  Google Scholar 

  • Supriatna, J., Froehlich, J. W., Erwin, J., & Southwick, C. (1992). Population, habitat and conservation status of Macaca maurus, Macaca tonkeana and their putative hybrids. Tropical Biodiversity, 1, 31–48.

    Google Scholar 

  • Sussman, R. W., & Tattersall, I. (1981). Behavior and ecology of Macaca fascicularis in Mauritius: A preliminary study. Primates, 22, 192–205. doi:10.1007/BF02382610.

    Article  Google Scholar 

  • Sussman, R. W., & Tattersall, I. (1986). Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern Indian Ocean. Folia Primatologica, 46, 28–43.

    Article  Google Scholar 

  • Tosi, A. J., & Coke, C. S. (2007). Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques. Molecular Phylogenetics and Evolution, 42, 498–504. doi:10.1016/j.ympev.2006.08.002.

    Article  PubMed  CAS  Google Scholar 

  • Tosi, A. J., Morales, J. C., & Melnick, D. J. (2000). Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution, 17, 133–144. doi:10.1006/mpev.2000.0834.

    Article  PubMed  CAS  Google Scholar 

  • Tosi, A. J., Morales, J. C., & Melnick, D. J. (2002). Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. International Journal of Primatology, 23, 161–178. doi:10.1023/A:1013258109954.

    Article  Google Scholar 

  • Tosi, A. J., Morales, J. C., & Melnick, D. J. (2003). Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution; International Journal of Organic Evolution, 57, 1419–1435.

    PubMed  CAS  Google Scholar 

  • Viray, J., Rolfs, B., & Smith, D. G. (2001). Comparison of the frequencies of major histocompatibility (MHC) class-II DQA1 and DQB1 alleles in Indian and Chinese rhesus macaques (Macaca mulatta). Comparative Medicine, 51, 555–561.

    PubMed  CAS  Google Scholar 

  • Weir, B. S. (1996). Genetic Data Analysis II. MA: Sinauer, Sunderland.

    Google Scholar 

  • Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution; International Journal of Organic Evolution, 38, 1358–1370. doi:10.2307/2408641.

    Google Scholar 

  • Wiseman, R. W., Wojcechowskyj, J. A., Greene, J. M., Blasky, A. J., Gopon, T., Soma, T., et al. (2007). Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. Journal of Virology, 81, 349–361. doi:10.1128/JVI.01841-06.

    Article  PubMed  CAS  Google Scholar 

  • Wolf, P. G., & Soltis, P. S. (1992). Estimates of gene flow among populations, geographic races, and species in the Ipomopsis aggregata complex (Polemoniaceae). Genetics, 130, 639–647.

    PubMed  CAS  Google Scholar 

  • Wright, S. (1951). The genetical structure of populations. Annals of Eugenics, 15, 323–354.

    Google Scholar 

  • Wright, S. (1978). In Evolution and the Genetics of Populations, Vol. 4. University of Chicago Press, Chicago, pp. 79–90.

  • Yeh, F. C., & Boyle, T. J. B. (1997). Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belgian Journal of Botany, 129, 157.

    Google Scholar 

  • Zhang, Y. P., & Shi, L. (1993). Phylogeny of rhesus monkeys (Macaca mulatta) as revealed by mitochondrial DNA restriction enzyme analysis. International Journal of Primatology, 14, 587–605. doi:10.1007/BF02215449.

    Article  Google Scholar 

Download references

Acknowledgments

We thank our former and current technicians at the Molecular Anthropology Laboratory, Department of Anthropology, University of California, Davis, for their contributions in compiling the genetic data used in the study. We thank all the facilities listed in Smith and McDonough (2005), Smith et al. (2006, 2007) and Satkoski et al. (2007) that have contributed samples used in this study. We also thank Robert Stallman (Department of Anthropology, University of California, Davis) and 2 anonymous reviewers for their helpful comments on improving the manuscript. A National Institutes of Health grant (no. RR05090 awarded to D. G. Smith) supported the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sree Kanthaswamy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kanthaswamy, S., Satkoski, J., George, D. et al. Hybridization and Stratification of Nuclear Genetic Variation in Macaca mulatta and M. fascicularis . Int J Primatol 29, 1295–1311 (2008). https://doi.org/10.1007/s10764-008-9295-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-008-9295-0

Keywords

Navigation