Skip to main content
Log in

Identification of Country of Origin and Admixture Between Indian and Chinese Rhesus Macaques

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

We describe a restriction analysis that distinguishes between rhesus macaques of unmixed Indian and Chinese ancestry and between western and eastern Chinese ancestry. We amplified a 254-bp fragment of mitochondrial DNA (mtDNA) that contains restriction sites hypothesized to be diagnostic of country of origin for samples from 534 and 567 individuals alleged to be of solely Indian or solely Chinese origin, respectively. After digestion with the MaeIII, SmlI, and BccI restriction enzymes, the polymerase chain reaction (PCR) products of only 3 of the 1101 samples exhibited restriction patterns uncharacteristic of their alleged country of origin. A sample comprising 392 of these rhesus macaques was genotyped for 24 nuclear microsatellite (STR) loci. Principal coordinates analysis confirmed marked genetic similarity of regional populations within each country but a substantial difference between Indian and Chinese rhesus macaques. Using STRUCTURE (Pritchard and Wen, 2003),we assigned probabilities of Chinese and Indian ancestry to each sample based on its STR genotypes. We assigned all the unmixed rhesus macaques to their correct countries of origin with probabilities >0.95. We constructed an artificial sample of 1st-generation hybrid Indian/Chinese rhesus macaques by randomly sampling from the genotypes of Indian and Chinese individuals. STRUCTURE assigned robabilities of Chinese and Indian ancestry to hybrids that closely corresponded with the proportions of alleles in that sample drawn from unmixed Chinese and Indian rhesus macaques.

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., and Thierry, B. (2002). Macaque evolution and dispersal in insular south-east Asia. Biol. J. Linnean Soc. 75: 555–576.

    Article  Google Scholar 

  • Arnason, U., Gullberg, A., Burquete, A. S., and Janke, A. (2000). Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Hereditas 133: 217–228.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, S. A., Bankier, T., Barrell, B. G., DeBruijn, M. H. L., Coulson, A. R., et al. (1981). Sequence and organization of the human mitochondrial genome. Nature 290: 457–465.

    Article  PubMed  CAS  Google Scholar 

  • Capitanio, J. P. (1986). Behavioral pathology. In Mitchell, G., and Erwin, J. (eds.), Comparative Primate Biology: Vol. 2A. Behavior, Conservation, and Ecology, New York, Alan R. Liss, pp. 411–454.

  • Capitanio, J. P., Mendoza, S. P., and Lerche, N. W. (1998). Individual differences in peripheral blood immunological and hormonal measures in adult male rhesus macaques (Macaca mulatta): Evidence for temporal and situational consistency. Am. J. Primatol. 44: 29–46.

    Article  PubMed  CAS  Google Scholar 

  • Champoux, M., Higley, J. D., and Soumi, S. J. (1997). Behavioral and physiological characteristics of Indian and Chinese-Indian hybrid rhesus macaque infants. Dev. Psychobiol. 31: 49–63.

    Article  PubMed  CAS  Google Scholar 

  • Champoux, M., Kriete, K. F., Higley, J. D., and Soumi, S. J. (1996). CBC and serum chemistry fifferences between Indian-derived and Chinese-Indian hybrid rhesus monkey infants. Am. J. Primatol. 39: 79–84.

    Article  Google Scholar 

  • Champoux, M., Soumi, S. J., and Schneider, M. L. (1994). Temperament differences between captive Indian and Chinese-Indian hybrid rhesus macaque neonates. Lab Anim. Sci. 44: 351–357.

    PubMed  CAS  Google Scholar 

  • Clarke, M. R., and O’Neil, J. A. S. (1999). Morphometric comparison of Chinese-origin and Indian-derived rhesus monkeys (Macaca mulatta). Am. J. Primatol. 47: 335–346.

    Article  PubMed  CAS  Google Scholar 

  • Deinard, A., and Smith, D. G. (2001). Phylogenetic relationships among the macaques: Evidence from the nuclear locus NRAMP1. J. Hum. Evol. 39: 1–15.

    Google Scholar 

  • Doxiadis, G. G. M., Otting, N., deGroot, N. G., deGroot, N., Rouweler, A. J. M., Noort, R., Verschoor, E. J., Bontjer, I., and 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 

  • Fooden, J. (1988). Taxonomy and evolution of the Sinica group of macaques. 6. Interspecific comparisons and synthesis. Field. Zool., n.s. 45: 1–44.

    Google Scholar 

  • Fooden, J. (2000). Systematic Review of the Rhesus Macaque, Macaca mulatta (Zimmermann, 1780). New Series, No. 96. Pub. 1509, Field Museum of Natural History Fieldiana, Chicago, p. 180.

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

  • Hayasaka, K., Fujii, K., and 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.

    PubMed  CAS  Google Scholar 

  • Joag, S. V., Stephens, E. B., Adams, R. J., Foresman, L., and Narayan, O. (1994). Pathogenesis of SIVMAC infection in Chinese and Indian rhesus macaques: Effects of spenectomy on virus burden. J. Virol. 200: 436–446.

    Article  CAS  Google Scholar 

  • Karanth, K. P. (2003). Evolution of disjunct distributions among wet-zone species of the Indian subcontinent: Testing various hypotheses using a phylogenetic approach. Curr. Sci. 85: 1276–1283.

    Google Scholar 

  • Ling, B., Veazey, R. S., Luckay, A., Penedo, C., Xu, K., Lifson, J. D., and Marx, P. (2002). SIVmac pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS 16: 1489–1496.

    Article  PubMed  Google Scholar 

  • Kanthaswamy, S., and Smith, D. G. (1998). Use of microsatellite polymorphisms for paternity exclusion in Rhesus macaques (Macaca mulatta). Primates 39: 135–145.

    Article  Google Scholar 

  • Kanthaswamy, S., and Smith, D. G. (2004). Effects of geographic origins on captive Macaca mulatta mtDNA variation. Comp. Med. (in press).

  • Marmi, J., Bertranpetit, J., Terradas, J., Takenaka, O., and Domingo-Roura, X. (2004). Radiation and phylogeography in the Japanese macaque, Macaca fuscata. Mol. Phylogenet. Evol. 30: 676–685.

    Article  PubMed  CAS  Google Scholar 

  • Melnick, D. J., Hoelzer, G. A., Absher, R., and Ashley, M. V. (1993). mtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol. Biol. Evol. 10: 282–295.

    PubMed  CAS  Google Scholar 

  • Morales, J. C., and Melnick, D. J. (1998). Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. J. Hum. Evol. 34: 1–23.

    Article  PubMed  CAS  Google Scholar 

  • Morin, P. A., Kanthaswamy, S., and Smith, D. G. (1997). Simple sequence repeat (SSR) polymorphisms for colony management and population genetics in rhesus macaques (Macaca mulatta). Am. J. Primatol. 42: 199–213.

    Article  PubMed  CAS  Google Scholar 

  • Morin, P. A., and Smith, D. G. (1995). Nonradioactive detection of hypervariable simple sequence repeats in short polyacrylamide gels. BioTechniques 19: 623–627.

    Google Scholar 

  • Peng, Y., Pan, R., Yu, F., Ye, Z., and Wang, H. (1993). Cranial comparisons between the populations of rhesus monkeys (Macaca mulatta) distribution in China and India. Acta Theriolog Sinica 13: 1–10.

    Google Scholar 

  • Pritchard, J. K., and Wen, W. (2003). Documentation for structure software (from http://pritch.bsd.uchicago.edu). Department of Human Genetics, Chicago, University of Chicago.

  • Schneider, M. L. (1992). The effect of mild stress during pregnancy on birthweight and neuromotor maturation in rhesus monkey infants (Macaca mulatta). Infant Behav. Dev. 15: 389–403.

    Article  Google Scholar 

  • Schneider, S., Roessli, D., and Excofflier, L. (2000). ARLEQUIN 2.001: A software for population genetic data analysis. Laboratory of Genetics and Biometry, University of Geneva, Switzerland.

  • Siegel, S., and Castellan, N. (1988). Nonparametrric Statistics for the Behavioral Sciences. McGraw-Hill, New York.

  • Smith, D. G. (1994). Genetic heterogeneity in five captive specific pathogen-free groups of rhesus macaques. Lab. Anim. Sci. 44: 200–210.

    PubMed  CAS  Google Scholar 

  • Smith, D. G., Kanthaswamy, S., Viray, J., and Cody, L. (2000). Additional highly polymorphic microsatellite (STR) loci for estimating kinship in rhesus macaques (Macaca mulatta). Am. J. Primatol. 50: 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Smith, D. G., and McDonough, J. W. (2005). Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am. J. Primatol. 65: 1–25.

    Article  PubMed  CAS  Google Scholar 

  • Smith, D. G., and Scott, L. M. (1989). Heterosis associated with regional crossbreeding between captive groups of rhesus macaques. Am. J. Primatol. 19: 255–260.

    Article  Google Scholar 

  • Tosi, A. J., Morales, J. C., and Melnick, D. J. (2000). Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Mol. Phyl. Evol. 17: 133–144.

    Article  CAS  Google Scholar 

  • Tosi, A. J., Morales, J. C., and Melnick, D. J. (2002). Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Istmus of Kra. Int. J. Primatol. 23: 161–178.

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • VandeBerg, J., and Williams-Blangero, S. (1997). Advantages and limitations of nonhuman primates as animal models in genetic research on complex diseases. J. Med. Primatol. 26: 113–119.

    PubMed  CAS  Google Scholar 

  • Viray, J., Rolfs, B., and 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). Comp. Med. 51: 555–561.

    PubMed  CAS  Google Scholar 

  • Williams-Blangero, S. (1993). Research-oriented genetic management of nonhuman primate colonies. Lab. Anim. Sci. 43: 535–540.

    PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

USPHS Grant RR05090 from the National Center for Research Resources, National Institutes of Health supported this study. We thank the facilities cited in Table 1 for providing samples for analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Glenn Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glenn Smith, D., George, D., Kanthaswamy, S. et al. Identification of Country of Origin and Admixture Between Indian and Chinese Rhesus Macaques. Int J Primatol 27, 881–898 (2006). https://doi.org/10.1007/s10764-006-9026-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-006-9026-3

KEY WORDS

Navigation