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Selective breeding of primates for use in research: consequences and challenges

Published online by Cambridge University Press:  01 January 2023

P Honess ,
M-A Stanley-Griffiths ,
S Narainapoulle ,
S Naiken  and
T Andrianjazalahatra
P Honess*
Affiliation:
Oxford University Veterinary Services, Parks Road, Oxford OX1 3PT, UK School of Veterinary Medicine and Science, Sutton Bonington, University of Nottingham, UK
M-A Stanley-Griffiths
Affiliation:
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius
S Narainapoulle
Affiliation:
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius
S Naiken
Affiliation:
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius
T Andrianjazalahatra
Affiliation:
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius
*
* Contact for correspondence and requests for reprints: paul.honess@vet.ox.ac.uk
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Abstract

Primates are bred in captivity for a number of purposes, from zoo-based captive breeding programmes for conservation to breeding for biomedical research. In each case, breeding animals that are fit for purpose, either as viable candidates for reintroduction or as valid research models, has presented challenges and resulted in steep learning curves. The breeding of animals for biomedical research has become increasingly focused on the production of animals that are less stressed by captive (specifically laboratory) environments. This is because elevated, particularly chronic, stress responses can result in altered physiological, neurological and behavioural states that have the potential to compromise the validity of scientific results. Selective breeding in captivity to, for example, maximise production, select for docile temperament or specific genotypes for biomedical research, is likely to be counter to natural selective pressures for evolutionary fitness. Given that many natural selective pressures active in the wild are absent in captivity, this paper reviews the selective breeding of primates (especially Old World monkeys) in captivity, its potential negative effects, and options that exist for ameliorating these negative effects.

Keywords

animal welfarebiomedical researchbreeding facilitiesmacaquesOld World primatesselective breeding
Type
Research Article
Information
Animal Welfare , Volume 19 , Issue S1: Proceedings of the UFAW International Symposium ‘Darwinian selection, selective breeding and the welfare of animals’ Bristol, 2009 , May 2010 , pp. 57 - 65
Copyright
© 2010 Universities Federation for Animal Welfare

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References

Anderson, DM and Simpson, MJA 1979 Breeding performance of a captive colony of rhesus macaques (Macaca mulatta). Laboratory Animals 13: 275–281CrossRefGoogle Scholar
Anderson, JR and Chamove, AS 1984 Allowing captive primates to forage. Standards in Laboratory Animal Management, Part 2 pp 253–256. UFAW: Wheathampstead, Herts, UKGoogle Scholar
Bercovitch, FB 2002 Sex-biased parental investment in primates. International Journal of Primatology 23(4): 905–921CrossRefGoogle Scholar
Boot, R, Leussink, AB and Vlug, RF 1985 Influence of housing conditions on pregnancy outcome in cynomolgus monkeys (Macaca fascicularis). Laboratory Animals 19(1): 42–47CrossRefGoogle Scholar
Bourne, GH and Golarz de Bourne, MN 1975 Breeding monkeys for biomedical research. In: Bourne, GH (ed) The Rhesus Monkey, Volume III: Management, Reproduction and Pathology. Academic Press: London, UKGoogle Scholar
Brown, JL and Eklund, A 1994 Kin recognition and the major histocompatibility complex: An integrative review. The American Naturalist 143(3): 435–461Google Scholar
Carey, D, Kammerer, CM, Shade, RE, Rice, KS and McGill, HC Jr 1993 Selective breeding to develop lines of baboons with high and low blood pressure. Hypertension 21(6): 1076–1079CrossRefGoogle ScholarPubMed
Carlsson, HE, Schapiro, SJ, Farah, I and Hau, J 2004 Use of primates in research: A global overview. American Journal of Primatology 63(4): 225–237CrossRefGoogle ScholarPubMed
Chan, AWS, Chong, KY, Martinovich, C, Simerly, C and Schatten, G 2001 Transgenic monkeys produced by retroviral gene transfer into mature oocytes. Science 291(5502): 309–312CrossRefGoogle ScholarPubMed
Coffman, BS, Hess, WR, Glander, KE, Feeser, PE and Simons, EL 1993 Management of a breeding colony of aye-ayes (Daubentonia madagascariensis) at the Duke University Primate Center. AAZPA Regional Conference Proceedings 1993. American Association of Zoological Parks and Aquariums pp 161–167. 2-4 May 1993, Pittsburgh, PA, USAGoogle Scholar
Coleman, K, Tully, LA and McMillan, JL 2005 Temperament correlates with training success in adult rhesus macaques. American Journal of Primatology 65(1): 63–71CrossRefGoogle ScholarPubMed
Cowlishaw, G and Dunbar, RIM 1991 Dominance rank and mating success in male primates. Animal Behaviour 41: 1045–1056CrossRefGoogle Scholar
Crockett, CM, Shimoji, M and Bowden, DM 2000 Behavior, appetite, and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation. American Journal of Primatology 52(2): 63–803.0.CO;2-K>CrossRefGoogle ScholarPubMed
Cyranoski, D 2009 Marmoset model takes centre stage. Nature 459(7246): 492CrossRefGoogle ScholarPubMed
Dawson, JC, Dawson, WW, Cunningham, BE and Lambrou, GN 2003 Developing open angle intraocular hypertension: Early results of selective breeding in the Florida Monkey Colony. Investigative Ophthalmology and Visual Science 44(5): 1118.Google Scholar
De, Ruiter Jr, van Hooff, JARAM and Scheffrahn, W 1994 Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129: 203–224Google Scholar
Dewsbury, DA 2006 Monkey farm. A history of the Yerkes Laboratories of Primate Biology, Orange Park, Florida 1930-1965. Bucknell University Press: Lewisburg, PA, USAGoogle Scholar
Drevon-Gaillot, E, Perron-Lepage, M-F, Clément, C and Burnett, R 2006 A review of background findings in cynomolgus monkeys (Macaca fascicularis) from three different geographical origins. Experimental and Toxicologic Pathology 58(2-3): 77–88CrossRefGoogle ScholarPubMed
Fooden, J 1991 Systematic review of Philippine macaques (primates cercopithecidae: Macaca fascicularis sub spp). Fieldiana Zoology 64: 1–44Google Scholar
Fooden, J 2000 Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann 1780). Fieldiana Zoology 96: 1–180Google Scholar
Fridman, EP 2002 Medical primatology: History, biological foundations and applications. Taylor & Francis: London, UKCrossRefGoogle Scholar
Goin, DL and Gust, DA 1998 Peer-rearing influences subsequent maternal behavior and infant survival in a newly formed herpes B-virus negative rhesus macaque group. Primates 39(4): 539–543CrossRefGoogle Scholar
Goo, GP and Fugate, JK 1984 Effects of weaning on age on maternal reproduction and offspring health in rhesus monkeys (M. mulatta). Laboratory Animal Science 34: 66–69Google Scholar
Gouzoules, S and Gouzoules, H 1987 Kinship. In: Smuts, B, Cheney, D, Seyfarth, R, Wrangham, R and Struhsaker, T (eds) Primate Societies pp 299–305. University of Chicago Press: Chicago, USAGoogle Scholar
Goy, RW 1992 The mating behavior of primates: Estrus or sexuality. In: Itoigawa N, Sugiyama Y, Sackett GP and Thompson GKR (eds). Topics in Primatology: Behavior, Ecology, and Conservation, Volume 2 pp 151–161. University of Tokyo Press: Tokyo, JapanGoogle Scholar
Groves, CP 2001 Primate Taxonomy. Smithsonian Institution Press: Washington, USAGoogle Scholar
Ha, JC, Robinette, RL, Almasy, L and Dyke, B 2002 Genetics and caging type affect birth weight in captive pigtailed macaques (Macaca nemestrina). American Journal of Primatology 56: 207–213CrossRefGoogle Scholar
Ha, JC, Robinette, RL and Davis, A 2000 Survival and reproduction in the first two years following a large-scale primate colony move and social reorganization. American Journal of Primatology 50(2): 131–1383.0.CO;2-D>CrossRefGoogle ScholarPubMed
Hendrickx, AG and Dukelow, WR 1995 Breeding. In: Taylor Bennett, B, Abee, CR and Hendrickson, R (eds) Nonhuman Primates in Biomedical Research: Biology and Management pp 428. Academic Press: London, UKGoogle Scholar
Higley, J and Suomi, S 1989 Temperamental reactivity in nonhuman primates. In: Kohnstamm, G, Bates, J and Rothbart, M (eds) Temperament in Childhood pp 153–167. Wiley: New York, USAGoogle Scholar
Hill, DA and Okayasu, N 1996 Determinants of dominance among female macaques: Nepotism, demography and danger. In: Fa, JE and Lindburg, DG (eds) Evolution and Ecology of Macaque Societies pp 459–472. Cambridge University Press: Cambridge, UKGoogle Scholar
Hobbs, KR 1989 The SICONBREC project: Conditioning and breeding facilities for the cynomolgus monkey (Macaca fascicularis) in the Philippines: A review after the first five years. Animal Technology 40(1): 55–68Google Scholar
Honess, PE and Marin, CM 2006a Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience and Biobehavioral Reviews 30(3): 390–412CrossRefGoogle Scholar
Honess, PE and Marin, CM 2006b Enrichment and aggression in primates. Neuroscience and Biobehavioral Reviews 30(3): 413–436CrossRefGoogle Scholar
Jennings, M, Prescott, MJ, Buchanan-Smith, HM, Gamble, MR, Gore, M, Hawkins, P, Hubrecht, R, Hudson, S, Jennings, M, Keeley, JR, Morris, K, Morton, DB, Owen, S, Pearce, PC, Prescott, MJ, Robb, D, Rumble, RJ, Wolfensohn, S and Buist, D 2009 Refinements in husbandry, care and common procedures for non-human primates: Ninth report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Laboratory Animals 43(Supplement 1): 1–47CrossRefGoogle Scholar
Johnsen, DO 1995 History. In: Taylor Bennett, B, Abee, CR and Hendrickson, R (eds) Nonhuman Primates in Biomedical Research: Biology and Management pp 428. Academic Press: London, UKGoogle Scholar
Kappeler, PM and Van Schaik, CP 2004 Sexual selection in primates: review and preview. In: Kappeler, PM and Van Schaik, CP (eds) Sexual Selection in Primates. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Kleiman, DG, Beck, BB, Dietz, JM, Dietz, LA, Ballou, JD and Coimbra-Filho, AF 1986 Conservation program for the golden lion tamarin: Captive research and management, ecological studies, education strategies, and reintroduction. In: Benirschke, K (ed) Primates: The Road to Self-Sustaining Populations pp 959–979. Springer-Verlag: New York, USACrossRefGoogle Scholar
Knapp, LA, Ha, JC and Sackett, GP 1996 Parental MHC antigen sharing and pregnancy wastage in captive pigtailed macaques. Journal of Reproductive Immunology 32: 73–88CrossRefGoogle ScholarPubMed
Kotera, S, Tanaka, T, Tajima, Y and Nomura, T 1975 Establishment of an island breeding colony of Japanese monkeys as a laboratory animal. Laboratory Animal Handbooks 6: 95–105Google Scholar
Kyes, RC 1993 Survey of the long-tailed macaques introduced onto Tinjil Island, Indonesia. American Journal of Primatology 31(1): 77–83CrossRefGoogle ScholarPubMed
Latham, NR and Mason, GJ 2008 Maternal deprivation and the development of stereotypic behaviour. Applied Animal Behaviour Science 110(1-2): 84–108CrossRefGoogle Scholar
Lawler, SH, Sussman, RW and Taylor, LL 1995 Mitochondrial DNA of the Mauritian macaques (Macaca fascicularis): An example of the founder effect. American Journal of Physical Anthropology 96(2): 133–141CrossRefGoogle ScholarPubMed
Lee, PC 1996 The meanings of weaning: Growth, lactation, and life history. Evolutionary Anthropology 5(3): 87–983.0.CO;2-T>CrossRefGoogle Scholar
Lee, PC 1999 Comparative ecology of post natal growth and weaning among haplohrine primates. In: Lee, PC (ed) Comparative Primate Socioecology pp 111–136. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Lehman, SM and Taylor, LL 1992 Natural migration patterns predict escapes from a colony of Japanese macaques (Macaca fuscata). Laboratory Primate Newsletter 31(3): 3–8Google Scholar
Ling, B, Veazey, RS, Luckay, A, Penedo, C, Xu, K, Lifson, JD and Marx, PA 2002 SIVmac pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS 16: 1489–1496CrossRefGoogle Scholar
Mansfield, K 2005 Development of specific pathogen free nonhuman primate colonies. In: Wolfe-Coote, S (ed) The Laboratory Primate pp 621. Elsevier Academic Press: London, UKGoogle Scholar
McGill, HC Jr, McMahan, CA, Mott, GE, Marinez, YN and Kuehl, TJ 1988 Effects of selective breeding on the cholesterolemic responses to dietary saturated fat and cholesterol in baboons. Arteriosclerosis, Thrombosis, and Vascular Biology 8(1): 33–39Google ScholarPubMed
McGinley, MA 1984 The adaptive value of male-biased sex ratios among stressed animals. The American Naturalist 124(4): 597–599CrossRefGoogle Scholar
Mee, ET, Badhan, A, Karl, JA, Wiseman, RW, Cutler, K, Knapp, LA, Almond, N, O’Connor, DH and Rose, NJ 2009 MHC haplo-type frequencies in a UK breeding colony of Mauritian cynomolgus macaques mirror those found in a distinct population from the same geographic origin. Journal of Medical Primatology 38(1): 1–14CrossRefGoogle Scholar
Mehlman, PT, Higley, JD, Faucher, I, Lilly, AA, Taub, DM, Vickers, J, Suomi, SJ and Linnoila, M 1994 Low CSF 5-HIAA concentrations and severe aggression and impaired impulse control in nonhuman primates. American Journal of Psychiatry 151(10): 1485–1491Google ScholarPubMed
Melnick, D, Pearl, M and Richard, A 1984 Male migration and inbreeding avoidance in wild rhesus monkeys. American Journal of Primatology 7: 229–243CrossRefGoogle ScholarPubMed
Mineka, S and Suomi, SJ 1978 Social separation in monkeys. Psychological Bulletin 85(6): 1376–1400CrossRefGoogle ScholarPubMed
Mineka, S, Gunnar, M and Champoux, M 1986 Control and early socioemotional development: Infant rhesus monkeys reared in controllable versus uncontrollable environments. Child Development 57(5): 1241–1256.CrossRefGoogle Scholar
Mooney, JC and Lee, PC 1999 Reproductive parameters in woolly monkeys (Lagothrix lagotricha). Zoo Biology 18: 421–427.3.0.CO;2-6>CrossRefGoogle Scholar
Morton, WR, Kyes, KB, Kyes, RC, Swindler, DR and Swindler, KE 2005 Use of the primate model in research. In: Wolfe-Coote, S (ed) The Laboratory Primate pp 405–415. Elsevier Academic Press: London, UKGoogle Scholar
Nagarajan, P, Venatesan, R, Mahesh Kumar, MJ and Majumdar, SS 2004 Suppression of lactation in post-weaning Macaca radiata females by bromocriptine under laboratory conditions. Laboratory Primate Newsletter 43(1): 12–13Google Scholar
Novak, MA and Suomi, SJ 1988 Psychological well-being of primates in captivity. American Psychologist 43(10): 765–773CrossRefGoogle ScholarPubMed
NRC (National Research Council) 1996 Guide for the Care and Use of Laboratory Animals. National Academic Press: Washington DC, USAGoogle Scholar
Poole, TB 1997 Happy animals make good science. Laboratory Animals 31: 116–124CrossRefGoogle ScholarPubMed
Prescott, M and Jennings, M 2004 Ethical and welfare implications of the acquisition and transport of non-human primates for use in biomedical research and testing. ATLA 32(Supplement 1): 323–327Google ScholarPubMed
Price, KC and Coe, CL 2000 Maternal constraint on fetal growth patterns in the rhesus monkey (Macaca mulatta): The intergenerational link between mothers and daughters. Human Reproduction 15(2): 452–457CrossRefGoogle ScholarPubMed
Reinhardt, V 2002 Artificial weaning of Old World monkeys: Benefits and costs. Journal of Applied Animal Welfare Science 5(2): 151–156CrossRefGoogle ScholarPubMed
Reinhardt, V and Reinhardt, A 2000 Social enhancement for adult nonhuman primates in research laboratories: A review. Laboratory Animal 29(1): 34–41Google Scholar
Sasaki, E, Suemizu, H, Shimada, A, Hanazawa, K, Oiwa, R, Kamioka, M, Tomioka, I, Sotomaru, Y, Hirakawa, R, Eto, T, Shiozawa, S, Maeda, T, Ito, M, Ito, R, Kito, C, Yagihashi, C, Kawai, K, Miyoshi, H, Tanioka, Y, Tamaoki, N, Habu, S, Okano, H and Nomura, T 2009 Generation of transgenic non-human primates with germline transmission. Nature 459(7246): 523–527CrossRefGoogle ScholarPubMed
Satkoski, J, George, D, Smith, DG and Kanthaswamy, S 2008 Genetic characterization of wild and captive rhesus macaques in China. Journal of Medical Primatology 37(2): 67–80CrossRefGoogle ScholarPubMed
Shively, CA, Friedman, DP, Gage, HD, Bounds, MC, Brown-Proctor, C, Blair, JB, Henderson, JA, Smith, MA and Buchheimer, N 2006 Behavioral depression and positron emission tomography-determined serotonin IA receptor binding potential in cynomolgus monkeys. Archives of General Psychiatry 63: 396–403CrossRefGoogle Scholar
Silk, JB 1983 Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. American Naturalist 121: 56–66CrossRefGoogle Scholar
Slierendregt, BL, Kenter, M, Otting, N, Anholts, J, Jonker, M and Bontrop, RE 1993 Major histocompatibility haplotypes in a breeding colony of chimpanzees (Pan troglodytes). Tissue Antigens 42(2): 55–61Google Scholar
Smith, DG 2005 Genetic characterization of Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). Comparative Medicine 55(3): 227–230Google Scholar
Smith, DG, McDonough, JW and George, DA 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: 182–198CrossRefGoogle ScholarPubMed
Stanley, MA 2003 The breeding of naturally occurring B virusfree cynomolgus monkeys (Macaca fascicularis) on the island of Mauritius. International Perspectives: The Future of Nonhuman Primate Resources pp 46–48. National Academies Press: Washington, USAGoogle Scholar
Sussman, R and Tattersall, I 1981 Behavior and ecology of Macaca fascicularis in Mauritius: A preliminary study. Primates 22(2): 192–205CrossRefGoogle Scholar
Tattersall, I, Dunaif, A, Sussman, RW and Jamieson, R 1981 Hematological and serum biochemical values in free-ranging Macaca fascicularis of Mauritius: Possible diabetes mellitus and correlation with nutrition. American Journal of Primatology 1(4): 413–419CrossRefGoogle ScholarPubMed
Tosi, AJ and Coke, CS 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(2): 498–504CrossRefGoogle ScholarPubMed
Trichel, A, Rajakumar, P and Murphy-Corb, M 2002 Species-specific variation in SIV disease progression between Chinese and Indian subspecies of rhesus macaque. Journal of Medical Primatology 31: 171–178CrossRefGoogle ScholarPubMed
Trivers, RL and Willard, DE 1973 Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90–92CrossRefGoogle ScholarPubMed
Tsuchida, J, Yoshida, T, Sanaki, T and Yasutomi, Y 2008 Maternal behaviour of laboratory-born, individually reared long-tailed macaques (Macaca fascicularis). Journal of the American Association for Laboratory Animal Science 47(5): 29–34Google Scholar
van Noordwijk, M and van Schaik, C 1999 The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40(1): 105–130CrossRefGoogle ScholarPubMed
Wallen, K, Goldfoot, DA and Goy, RW 1981 Peer and maternal influences on the expression of foot-clasp mounting by juvenile male rhesus monkeys. Developmental Psychobiology 14(4): 299–309CrossRefGoogle ScholarPubMed
Wallis, J and Valentine, B 2001 Early vs natural weaning in captive baboons: The effect on timing of postpartum estrus and next conception. Laboratory Primate Newsletter 40(1): 10–13Google Scholar
Watts, E and Meder, A 1996 Introduction and socialization techniques for primates. In: Kleiman, DG, Allen, ME, Thompson, KV and Lumpkin, S (eds) Wild Mammals in Captivity: Principles and Techniques pp 67–77. University of Chicago Press: Chicago, USAGoogle Scholar
Wolfe-Coote, S 2005 The Laboratory Primate. The Handbook of Experimental Animals. Blackwell Publications: Oxford, UKGoogle Scholar
Wolfensohn, SE 1997 Brief review of scientific studies of the welfare implications of transporting primates. Laboratory Animals 31(4): 303–305CrossRefGoogle ScholarPubMed
Wolfensohn, SE and Honess, PE 2005 Handbook of Primate Husbandry and Welfare. Blackwell Publications: Oxford, UKCrossRefGoogle Scholar
Yerkes, RM 1916 Provision for the study of monkeys and apes. Science 43(1103): 231–234CrossRefGoogle Scholar
Yerkes, RM 1935 Yale laboratories of primate biology, incorporated. Science 82(2139): 618–620CrossRefGoogle ScholarPubMed
Zumpe, D and Michael, R 1984 Low potency of intact male rhesus monkeys after long-term visual contact with their female partners. American Journal of Primatology 6: 241–252CrossRefGoogle ScholarPubMed
Zumpe, D and Michael, R 1996 Social factors modulate the effects of hormones on the sexual and aggressive behavior of macaques. American Journal of Primatology 38: 233–2613.0.CO;2-#>CrossRefGoogle ScholarPubMed