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Development of a microsatellite set for paternity assignment of captive rhesus macaques (Macaca mulatta) from Anhui Province, China

  • Animal Genetics
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Abstract

Microsatellites are playing an important role in paternity assignment of animals. Given the cost and effort, it would be optimal to develop a minimal microsatellite marker set for paternity testing. This study was the first to assess paternity in a captive colony of rhesus macaques (Macaca mulatta) from the Chinese province of Anhui using 10 polymorphic microsatellites. Results indicated that if at least 6 loci were genotyped, the probability of paternity assignment success was nearly 100%. Our results provide a panel of 6 markers that is effective for assessing paternity of subspecies M. m. siamica of Anhui origin.

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References

  1. Sauermann, U., Nürnberg, P., Bercovitch, F., et al., Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques, Hum. Genet., 2001, vol. 108, pp. 249–254.

    Article  PubMed  CAS  Google Scholar 

  2. Lane, M.A., Mattison, J., Ingram, D.K., and Roth, G.S., Caloric restriction and aging in primates: Relevance to humans and possible CR mimetics, Microsc. Res. Tech., 2002, vol. 59, pp. 335–338.

    Article  PubMed  Google Scholar 

  3. Moore, T., Killiany, R., Rosene, D., et al., Hypertension-induced changes in monoamine receptors in the prefrontal cortex of rhesus monkeys, Neuroscience, 2003, vol. 120, pp. 177–189.

    Article  PubMed  CAS  Google Scholar 

  4. Barr, C.S., Schwandt, M.L., Newman, T.K., and Higley, J.D.E.E., The use of adolescent nonhuman primates to model human alcohol intake: neurobiological, genetic, and psychological variables, Ann. N.Y. Acad. Sci., 2004, vol. 1021, pp. 221–233.

    Article  PubMed  CAS  Google Scholar 

  5. Golos, T.G., Pregnancy initiation in the rhesus macaque: towards functional manipulation of the maternal-fetal interface, Reprod. Biol. Endocrinol., 2004, vol. 2, p. 35.

    Article  PubMed  Google Scholar 

  6. Wolf, D.P., Assisted reproductive technologies in rhesus macaques, Reprod. Biol. Endocrinol., 2004, vol. 2, p. 37.

    Article  PubMed  Google Scholar 

  7. Frankham, B., Ballou, J.D., and Briscoe, D.A., Introduction to Conservation Genetics, Cambridge: Cambridge Univ. Press, 2002.

    Book  Google Scholar 

  8. Frankham, R., Genetics and conservation biology, Biologies, 2003, vol. 326, pp. S22–S29.

    Article  PubMed  Google Scholar 

  9. Abee, C.R., Mansfield, K., Tardif, S.D., and Morris, T., Nonhuman Primates in Biomedical Research: Biology and Management, Academic Press, 2012.

    Google Scholar 

  10. Williams-Blangero, S., VandeBerg, J.L. and Dyke, B., Genetic management of nonhuman primates, J. Med. Primatol., 2002, vol. 31, pp. 1–7.

    Article  PubMed  Google Scholar 

  11. Litt, M. and Luty, J.A., A hypervariable microsatellite revealed by in vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene, Am. J. Hum. Genet., 1989, vol. 44, pp. 397–401.

    PubMed  CAS  Google Scholar 

  12. Ellegren, H., Microsatellites: simple sequences with complex evolution, Nat. Rev. Genet., 2004, vol. 5, pp. 435–445.

    Article  PubMed  CAS  Google Scholar 

  13. Kayser, M., Ritter, H., Bercovitch, F., et al., Identification of highly polymorphic microsatellites in the rhesus macaque Macaca mulatta by cross-species amplification, Mol. Ecol., 1996, vol. 5, pp. 157–159.

    Article  PubMed  CAS  Google Scholar 

  14. Kanthaswamy, S. and Smith, D.G., Use of microsatellite polymorphisms for paternity exclusion in rhesus macaques (Macaca multatta), Primates, 1998, vol. 39, pp. 135–145.

    Article  Google Scholar 

  15. Nair, S., Ha, J., and Rogers, J., Nineteen new microsatellite DNA polymorphisms in pigtailed macaques (Macaca nemestrina), Primates, 2000, vol. 41, pp. 343–350.

    Article  Google Scholar 

  16. Newman, T.K., Fairbanks, L.A., Pollack, D., and Rogers, J., Effectiveness of human microsatellite loci for assessing paternity in a captive colony of vervets (Chlorocebus aethiops sabaeus), Am. J. Primatol., 2002, vol. 56, pp. 237–243.

    Article  PubMed  Google Scholar 

  17. Seyedabadi, H., Amirinia, C., Banabazi, M.H., and Emrani, H., Parentage verification of Iranian Caspian horse using microsatellites markers, Iran. J. Biotechnol., 2006, vol. 4, pp. 260–263.

    CAS  Google Scholar 

  18. Tian, F., Sun, D., and Zhang, Y., Establishment of paternity testing system using microsatellite markers in Chinese Holstein, J. Genet. Genomics, 2008, vol. 35, pp. 279–284.

    Article  PubMed  CAS  Google Scholar 

  19. Godavarthi, S., Jayaraman, A., and Gaur, A., Cross-species amplification of human microsatellite markers in pig-tailed and stump-tailed macaques, J. Genet., 2010, vol. 90, pp. 1–4.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  22. Hadfield, R.M., Pullen, J.G., Davies, K.F., et al., Toward developing a genome-wide microsatellite marker set for linkage analysis in the rhesus macaque (Macaca mulatta): identification of 76 polymorphic markers, Am. J. Primatol., 2001, vol. 54, pp. 223–231.

    Article  PubMed  CAS  Google Scholar 

  23. Rogers, J., Garcia, R., Shelledy, W., et al., An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci, Genomics, 2006, vol. 1 p, pp. 30–38.

    Article  Google Scholar 

  24. Penedo, M.C.T., Bontrop, R.E., Heijmans, C.M.C., et al., Microsatellite typing of the rhesus macaque MHC region, Immunogenetics, 2005, vol. 57, pp. 198–209.

    Article  PubMed  CAS  Google Scholar 

  25. Blanquer-Maumont, A. and Crouau-Roy, B., Polymorphism, monomorphism, and sequences in conserved microsatellites in primate species, J. Mol. Evol., 1995, vol. 41, pp. 492–497.

    Article  PubMed  CAS  Google Scholar 

  26. Garza, J.C., Slatkin, M., and Freimer, N.B., Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size, Mol. Biol. Evol., 1995, vol. 12, pp. 594–603.

    PubMed  CAS  Google Scholar 

  27. Crouau-Roy, B., Slatkin, M., and Freimer, N., A finescale comparison of the human and chimpanzee genomes: linkage, linkage disequilibrium and sequence analysis, Hum. Mol. Genet., 1996, vol. 5, pp. 1131–1137.

    Article  PubMed  CAS  Google Scholar 

  28. Brandon-Jones, D., Eudey, A., Geissmann, T., et al., Asian primate classification, Int. J. Primatol., 2004, vol. 25, pp. 97–164.

    Article  Google Scholar 

  29. Kalinowski, S.T., Taper, M.L., and Marshall, T.C., Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment, Mol. Ecol., 2007, vol. 16, pp. 1099–1106.

    Article  PubMed  Google Scholar 

  30. Rousset, F., GENEPOP’007: a complete re-implementation of the Genepop software for Windows and Linux, Mol. Ecol. Resour., 2008, vol. 8, pp. 103–106.

    Article  PubMed  Google Scholar 

  31. Jakabova, D., Trandik, J., Chrastina, J., et al., Effectiveness of six highly polymorphic microsatellite markers in resolving paternity cases inoroughbred horses in Slovakia, Czech J. Anim. Sci., 2002, vol. 12, pp. 497–501.

    Google Scholar 

  32. Chambers, K.E., Reichard, U.H., Möller, A., et al., Cross-species amplification of human microsatellite markers using noninvasive samples from white-handed gibbons (Hylobates lar), Am. J. Primatol., 2004, vol. 64, pp. 19–27.

    Article  PubMed  Google Scholar 

  33. Bradley, B.J., Doran-Sheehy, D.M., and Vigilant, L., Potential for female kin associations in wild western gorillas despite female dispersal, Proc. R. Soc. London, Ser. B, 2007, vol. 274, pp. 2179–2185.

    Article  Google Scholar 

  34. George, D.D.P.F., Human short tandem repeat (STR) markers for paternity testing in pig-tailed macaques, HAYATI J. Biosci., 2007, vol. 14, pp. 39–43.

    Google Scholar 

  35. Farajallah, D.P., Human short tandem repeat (STR) markers for paternity testing in pig-tailed macaques, HAYATI J. Biosci., 2009, vol. 14, pp. 39–43.

    Google Scholar 

  36. Sherman, G., Kachman, S., Hungerford, L., et al., Impact of candidate sire number and sire relatedness on DNA polymorphism-based measures of exclusion probability and probability of unambiguous parentage, Anim. Genet., 2004, vol. 35, pp. 220–226.

    Article  PubMed  CAS  Google Scholar 

  37. Storz, J.F., Beaumont, M.A., and Alberts, S.C., Genetic evidence for long-term population decline in a savannah-dwelling primate: Inferences from a hierarchical Bayesian model, Mol. Biol. Evol., 2002, vol. 19, pp. 1981–1990.

    Article  PubMed  CAS  Google Scholar 

  38. Clisson, I., Lathuilliere, M., and Crouau-Roy, B., Conservation and evolution of microsatellite loci in primate taxa, Am. J. Primatol., 2000, vol. 50, pp. 205–214.

    Article  PubMed  CAS  Google Scholar 

  39. Kawamoto, Y., Kawamoto, S., Matsubayashi, K., et al., Genetic diversity of longtail macaques (Macaca fascicularis) on the island of Mauritius: an assessment of nuclear and mitochondrial DNA polymorphisms, J. Med. Primatol., 2008, vol. 37, pp. 45–54.

    PubMed  CAS  Google Scholar 

  40. Kanthaswamy, S., Dollen, A., Kurushima, J.D., et al., Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta), Amer. J. Primatol., 2006, vol. 68, pp. 73–95.

    Article  CAS  Google Scholar 

  41. Coote, T., Bruford, M., Human microsatellites applicable for analysis of genetic variation in apes and Old World monkeys, J. Heredity, 1996, vol. 87, pp. 406–410.

    Article  CAS  Google Scholar 

  42. Numberg, P., Sauermann, U., Kayser, M., et al., Paternity assessment in rhesus macaques (Macaca mulatta): multilocus DNA fingerprinting and PCR marker typing, Amer. J. Primatol., 1998, vol. 44, pp. 1–18.

    Google Scholar 

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Correspondence to Y. R. Xu.

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Xu, Y.R., Li, J.H., Zhu, Y. et al. Development of a microsatellite set for paternity assignment of captive rhesus macaques (Macaca mulatta) from Anhui Province, China. Russ J Genet 49, 730–736 (2013). https://doi.org/10.1134/S1022795413070144

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  • DOI: https://doi.org/10.1134/S1022795413070144

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