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Population genetics of the California National Primate Research Center’s (CNPRC) captive Callicebus cupreus colony

Primates volume 56, pages 37–44 (2015)Cite this article

Abstract

The California National Primate Research Center maintains a small colony of titi monkeys (Callicebus cupreus) for behavioral studies. While short tandem repeat (STR) markers are critical for the genetic management of the center’s rhesus macaque (Macaca mulatta) breeding colony, STRs are not used for this purpose in the maintenance of the center’s titi monkey colony. Consequently, the genetic structure of this titi monkey population has not been characterized. A lack of highly informative genetic markers in titi monkeys has also resulted in scant knowledge of the species’ genetic variation in the wild. The purpose of this study was to develop a panel of highly polymorphic titi monkey STRs using a cross-species polymerase chain reaction (PCR) amplification protocol that could be used for the genetic management of the titi monkey colony. We screened 16 STR primer pairs and selected those that generated robust and reproducible polymorphic amplicons. Loci that were found to be highly polymorphic, very likely to be useful for parentage verification, pedigree assessment, and studying titi monkey population genetics, were validated using Hardy–Weinberg equilibrium and linkage disequilibrium analyses. The genetic data generated in this study were also used to assess directly the impact on the colony’s genetic diversity of a recent adenovirus outbreak. While the adenovirus epizootic disease caused significant mortality (19 deaths among the 65 colony animals), our results suggest that the disease exhibited little or no influence on the overall genetic diversity of the colony.

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References

  • Babb PL, McIntosh AM, Fernandez-Duque E, Di Fiore A, Schurr TG (2011) An optimized microsatellite genotyping strategy for assessing genetic identity and kinship in Azara’s owl monkeys (Aotus azarai). Folia Primatol 82:107–117. doi:10.1159/000330564

    Article  PubMed  Google Scholar 

  • Bailey C, Mansfield K (2010) Emerging and reemerging infectious diseases of nonhuman primates in the laboratory setting. Vet Pathol 47:462–481. doi:10.1177/0300985810363719

    Article  CAS  PubMed  Google Scholar 

  • Becker J, Baker AJ, Frampton T, Pullen PK, Bales KL, Mendoza SP, Mason WA (2013) Pitheciines in captivity: challenges and opportunities, past, present and future. In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of Titis, Sakis and Uacaris. Cambridge University Press, New York, pp 344–349

    Chapter  Google Scholar 

  • Chambers KE, Reichard UH, Moller A, Nowak K, Vigilant L (2004) Cross-species amplification of human microsatellite markers using noninvasive samples from white-handed gibbons (Hylobates lar). Am J Primatol 64:19–27. doi:10.1002/ajp.20058

    Article  PubMed  Google Scholar 

  • Chen EC, Yagi S, Kelly KR, Mendoza SP, Tarara RP, Canfield DR, Maninger N, Rosenthal A, Spinner A, Bales KL, Schnurr DP, Lerche NW, Chiu CY (2011) Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS Pathog 7:e1002155. doi:10.1371/journal.ppat.1002155

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Di Fiore A, Fleischer RC (2004) Microsatellite markers for woolly monkeys (Lagothrix lagotricha) and their amplification in other new world primates (Primates: Platyrrhini). Mol Ecol Notes 4:246–249. doi:10.1111/j.1471-8286.2004.00631.x

    Article  Google Scholar 

  • Ellsworth JA, Hoelzer GA (1998) Characterization of microsatellite loci in a new world primate, the mantled howler monkey (Alouatta palliata). Mol Ecol 7:657–658. doi:10.1046/j.1365-294X.1998.00340.x

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50. doi:10.4137/ebo.s0

    CAS  PubMed Central  Google Scholar 

  • Fernandez-Duque E, Valeggia CR, Mason WA (2000) Effects of pair-bond and social context on male-female interactions in captive titi monkeys (Callicebus moloch, Primates: Cebidae). Ethology 106:1067–1082. doi:10.1046/j.1439-0310.2000.00629.x

    Article  Google Scholar 

  • Goncalves EC, Silva A, Barbosa MSR, Schneider MPC (2004) Isolation and characterization of microsatellite loci in Amazonian red-handed howlers Alouatta belzebul (Primates, Plathyrrini). Mol Ecol Notes 4:406–408. doi:10.1111/j.1471-8286.2004.00667.x

    Article  CAS  Google Scholar 

  • Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1931–1938

    Google Scholar 

  • Gualda-Barros J, Nascimento FOd, Amaral MKd (2012) A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia (São Paulo) 52:261–279

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372. doi:10.2307/2532296

    Article  CAS  PubMed  Google Scholar 

  • Hershkovitz P (1988) Origin, speciation, and distribution of South American titi monkeys, genus Callicebus (Family Cebidae, Platyrrhini). Proc Acad of Natl Sci Phila 140:240–272. doi:10.2307/4064927

    Google Scholar 

  • Hershkovitz P (1990) Titis, new world monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zool n.s.:1–109

  • Hughes CR, Queller DC (1993) Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism. Mol Ecol 2:131–137. doi:10.1111/j.1365-294X.1993.tb00102.x

    Article  CAS  PubMed  Google Scholar 

  • Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Resour 10:6–30. doi:10.1111/j.1755-0998.2009.02778.x

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294X.2007.03089.x

    Article  PubMed  Google Scholar 

  • Kanthaswamy S, von Dollen A, Kurushima JD, Alminas O, Rogers J, Ferguson B, Lerche NW, Allen PC, Smith DG (2006) Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta). Am J Primatol 68:73–95. doi:10.1002/ajp.20207

    Article  CAS  PubMed  Google Scholar 

  • Kanthaswamy S, Satkoski J, Kou A, Malladi V, Smith DG (2010) Detecting signatures of inter-regional and inter-specific hybridization among the Chinese rhesus macaque specific pathogen-free (SPF) population using single nucleotide polymorphic (SNP) markers. J Med Primatol 39:252–265

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kanthaswamy S, Ng J, Penedo MC, Ward T, Smith DG, Ha JC (2012) Population genetics of the Washington National Primate Research Center’s (WaNPRC) captive pigtailed macaque (Macaca nemestrina) population. Am J Primatol 74:1017–1027. doi:10.1002/ajp.22055

    Article  PubMed  Google Scholar 

  • Kinzey WG (1981) The Titi Monkeys, Genus Callicebus. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and behavior of Neotropical Primates, vol 1. Academia Brasileira de Ciencias, Rio de Janeiro, pp 241–276

    Google Scholar 

  • Lorenz R, Mason WA (1971) Establishment of a colony of Titi monkeys. International Zoo Yearbook 11:168–174. doi:10.1111/j.1748-1090.1971.tb01896.x

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655. doi:10.1046/j.1365-294x.1998.00374.x

    Article  CAS  PubMed  Google Scholar 

  • Mason WA (1966) Social organization of the South Ameican monkey, Callicebus moloch: a preliminary report. Tulane stud zool 13:23–28

    Google Scholar 

  • Mendoza SP, Mason WA (1986) Contrasting responses to intruders and to involuntary separation by monogamous and polygynous new world monkeys. Physiol Behav 38:795–801

    Article  CAS  PubMed  Google Scholar 

  • Menescal LA, Goncalves EC, Silva A, Ferrari SF, Schneider MP (2009) Genetic diversity of red-bellied Titis (Callicebus moloch) from Eastern Amazonia based on microsatellite markers. Biochem Genet 47:235–240. doi:10.1007/s10528-008-9220-4

    Article  CAS  PubMed  Google Scholar 

  • Moore CM, Leland MM, Brzyski RG, McKeand J, Witte SM, Rogers J (1998) A baboon (Papio hamadryas) with an isochromosome for the long arm of the X. Cytogenet Cell Genet 82:80–82

    Article  CAS  PubMed  Google Scholar 

  • Muniz L, Vigilant L (2008) Permanent genetic resources: isolation and characterization of microsatellite markers in the white-faced capuchin monkey (Cebus capucinus) and cross-species amplification in other new world monkeys. Mol Ecol Resour 8:402–405. doi:10.1111/j.1471-8286.2007.01971.x

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rogers J, Bergstrom M, Garcia Rt, Kaplan J, Arya A, Novakowski L, Johnson Z, Vinson A, Shelledy W (2005) A panel of 20 highly variable microsatellite polymorphisms in rhesus macaques (Macaca mulatta) selected for pedigree or population genetic analysis. Am J Primatol 67:377–383. doi:10.1002/ajp.20192

    Article  CAS  PubMed  Google Scholar 

  • Smith KL, Alberts SC, Bayes MK, Bruford MW, Altmann J, Ober C (2000) Cross-species amplification, non-invasive genotyping, and non-Mendelian inheritance of human STRPs in Savannah baboons. Am J Primatol 51:219–227. doi:10.1002/1098-2345(200008)51:4<219:AID-AJP1>3.0.CO;2-G

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Bonvicino CR, Svartman M, Seuanez HN (2003) Chromosome painting in Callicebus lugens, the species with the lowest diploid number (2n = 16) known in primates. Chromosoma 112:201–206. doi:10.1007/s00412-003-0261-5

    Article  CAS  PubMed  Google Scholar 

  • Valeggia CR, Mendoza SP, Fernandez-Duque E, Mason WA, Lasley B (1999) Reproductive biology of female titi monkeys (Callicebus moloch) in captivity. Am J Primatol 47:183–195. doi:10.1002/(SICI)1098-2345(1999)47:3<183:AID-AJP1>3.0.CO;2-J

    Article  CAS  PubMed  Google Scholar 

  • van Roosmalen MGM, van Roosmalen T, Mittermeier RA (2002) A taxonomic review of the titi monkeys, genus Callicebus Thomas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neotrop Primates 10:1–52

    Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  CAS  Google Scholar 

  • Walling CA, Pemberton JM, Hadfield JD, Kruuk LE (2010) Comparing parentage inference software: reanalysis of a red deer pedigree. Mol Ecol 19:1914–1928. doi:10.1111/j.1365-294X.2010.04604.x

    Article  PubMed  Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations : a treatise in four volumes. University of Chicago Press, Chicago, London

    Google Scholar 

  • Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16. doi:10.1046/j.0962-1083.2001.01418.x

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the California National Primate Research Center (CNPRC) base Grant (OD000169-48), as well as grants from the Good Nature Institute to KB (HD053555 and HD071998). This research adhered to the American Society of Primatologists’ principles for the ethical treatment of primates. Animals used in this research were managed in compliance with Institutional Animal Care and Use Committee (IACUC) regulations or in accordance with the National Institutes of Health guidelines or the US Department of Agriculture regulations prescribing the humane care and use of laboratory animals. The University of California, Davis, and the California National Primate Research Center are AAALAC accredited. The authors are very grateful to the reviewers for their thorough and insightful comments, which considerably improved the manuscript.

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Authors and Affiliations

  1. University of California Graduate Program in Forensic Science, University of California, One Shields Ave, Davis, 95616, CA, USA

    Adrian Mendoza, David Glenn Smith & Sree Kanthaswamy

  2. Department of Anthropology, University of California, One Shields Ave, Davis, 956163, CA, USA

    Jillian Ng, Debra A. George, David Glenn Smith & Sree Kanthaswamy

  3. Department of Psychology, University of California, One Shields Ave, Davis, 95616, CA, USA

    Karen L. Bales & Sally P. Mendoza

  4. California National Primate Research Center, University of California, One Shields Ave, Davis, 95616, CA, USA

    Karen L. Bales, Sally P. Mendoza, David Glenn Smith & Sree Kanthaswamy

  5. Department of Environmental Toxicology, University of California, One Shields Ave, Davis, 95616, CA, USA

    Sree Kanthaswamy

  6. 303 Young Hall, Davis, 95616, CA, USA

    Sree Kanthaswamy

Authors
  1. Adrian Mendoza
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  2. Jillian Ng
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  3. Karen L. Bales
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  4. Sally P. Mendoza
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  5. Debra A. George
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  6. David Glenn Smith
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  7. Sree Kanthaswamy
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Correspondence to Sree Kanthaswamy.

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Mendoza, A., Ng, J., Bales, K.L. et al. Population genetics of the California National Primate Research Center’s (CNPRC) captive Callicebus cupreus colony. Primates 56, 37–44 (2015). https://doi.org/10.1007/s10329-014-0446-y

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  • DOI: https://doi.org/10.1007/s10329-014-0446-y

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