Inbreeding depression in non-human primates: A historical review of methods used and empirical data

American Journal of Primatology

Volumn 69, Issue 12, 2007, Pages 1370-1386

  Charpentier, M J E ^a,b   Widdig, A ^a,c,d   Alberts, S C ^a,e  

^a DUKE UNIVERSITY   (United States)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^d UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^e INSTITUTE OF PRIMATE RESEARCH   (Kenya)

Author keywords

Genetic analysis; Heterozygosity; Inbred mating; Inbreeding; Pedigrees; Primates

Indexed keywords

DETECTION METHOD; ESTIMATION METHOD; FITNESS; GENETIC ANALYSIS; INBREEDING DEPRESSION; PRIMATE; WILD POPULATION;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; DNA SEQUENCE; EMPIRICAL RESEARCH; FEMALE; GENETIC PROCEDURES; GENETICS; HETEROZYGOTE DETECTION; HISTORY; INBREEDING; MALE; PEDIGREE; PHYSIOLOGY; PRIMATE;

ANIMALS; BEHAVIOR, ANIMAL; EMPIRICAL RESEARCH; FEMALE; GENETIC TECHNIQUES; HETEROZYGOTE DETECTION; HISTORY, 20TH CENTURY; INBREEDING; MALE; MODELS, GENETIC; PEDIGREE; PRIMATES; SEQUENCE ANALYSIS, DNA;

PRIMATES;

EID: 36749068318     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20445     Document Type: Article

References (98)

1. Acevedo-Whitehouse K, Gulland F, Grieg D, Amos W. 2003. Inbreeding: disease susceptibility in California sea lions. Nature 422:35.
2. Alberts SC, Altmann J. 1995. Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279-306.
3. Alberts SC, Buchan JC, Altmann J. 2006. Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177-1196.
4. Altmann J, Alberts SC. 2003. Intraspecific variability in fertility and offspring survival in a nonhuman primate: behavioral control of ecological and social sources. In: Wachter KW, Bulatao RA, editors. Offspring: the biodemography of fertility and family behavior. Washington, DC: National Academy Press. p 140-169.
5. Altmann J, Alberts SC, Haines, SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Bruford M. 1996. Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93: 5797-5801.
6. Amos W, Worthington Wilmer J, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T. 2001. The influence of parental relatedness on reproductive success. Proc Roy Soc Lond B: Biol Sci 268:2021-2027.
7. Andayani N, Morales JC, Forstner MRJ, Supriatna J, Melnick DJ. 2001. Genetic variability in mtDNA of the silvery gibbon: implications for the conservation of a critically endangered species. Conserv Biol 15: 770-775.
8. Balloux F, Amos W, Coulson T. 2004. Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021-3031.
9. Barret SCH, Charlesworth D. 1991. Effect of a change in the level of inbreeding on the genetic load. Nature 352:522-524.
10. Beehner JC, Nguyen N, Wango EO, Alberts SC, Altmann J. 2006a. The ecology of conception and pregnancy failure in wild baboons. Horm Behav 49:688-699.
11. Beehner JC, Onderdonk DA, Alberts SC, Altmann J. 2006b. The ecology of conception and pregnancy failure in wild baboons. Behav Ecol 17:741-750.
12. Berard JD, Nürnberg P, Epplen JT, Schmidtke J. 1994. Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177-201.
13. Blouin SF, Blouin M. 1988. Inbreeding avoidance behaviors. Trends Ecol Evol 3:230-233.
14. Britten HB. 1996. Meta-analyses of the association between multilocus heterozygosity and fitness. Evolution 50:2158-2164.
15. Bulger J, Hamilton WJ. 1988. Inbreeding and reproductive success in a natural Chacma baboon (Papio cynocephalus ursinus) population. Anim Behav 36:574-578.
16. Burke T, Bruford MW. 1987. DNA fingerprinting in birds. Nature 327:149-152.
17. Bush M, Montali RJ, Kleiman DG, Randolph J, Abramowitz MD, Evans RF. 1980. Diagnosis and repair of familial diaphragmatic defects in golden lion tamarins. J Am Vet Med Assoc 177:858-862.
18. Chalifoux LV, Elliott MW. 1986. Congenital anomalies in two neonatal tamarins (Saguinus oedipus and Saguinus fuscicollis). J Med Primatol 15:329-337.
19. Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Sys 18: 237-268.
20. Charlesworth D, Charlesworth B. 1999. The genetic basis of inbreeding depression. Genet Res 74:329-340.
21. Charpentier M, Setchell JM, Prugnolle F, Knapp LA, Wickings EJ, Peignot P, Hossaert-McKey M. 2005a. Genetic diversity and reproductive success in mandrills (Mandrillus sphinx). Proc Natl Acad Sci USA 102:16723-16728.
22. Charpentier M, Hossaert-McKey M, Wickings EJ, Peignot P. 2005b. Consequences of a one-male harem reproductive system and inbreeding in a captive group of Cercopithecus solatus. Int J Primatol 26:697-710.
23. Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell JM, Wickings EJ. 2005c. Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behav Ecol 16: 614-623.
24. Charpentier M, Setchell JM, Prugnolle F, Wickings EJ, Peignot P, Balloux F, Hossaert-McKey M. 2006. Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx). Mol Ecol 15:21-28.
25. Coltman DW, Slate J. 2003. Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971-983.
26. Coltman DW, Bowen WD, Wright JM. 1998. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc Roy Soc Lond B: Biol Sci 265:803-809.
27. Constable JL, Ashley MV, Goodall J, Pusey AE. 2001. Noninvasive paternity assignment in Gombe chimpanzees. Mol ecol 10:1279-1300.
28. Coulson TN, Pemberton JM, Albon SD, Beaumont M, Marshall TC, Slate J, Guinness FE, Clutton-Brock TH. 1998. Microsatellites reveal heterosis in red deer. Proc Roy Soc Lond B: Biol Sci 267: 489-495.
29. Coulson TN, Albon SD, Slate J, Pemberton JM. 1999. Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53: 1951-1960.
30. Crawford MH, O'Rourke DH. 1978. Inbreeding, lymphoma, genetics and morphology of the Papio hamadryas colony of Sukhumi. J Med Primatol 7:355-360.
31. Crawford MH, O'Rourke DH, Dykes DD, Yakovleva LA, Voevodin AF, Lapin B, Polesky HF. 1984. Inbreeding, heterozygosity, and lymphoma risk among the baboons (Papio hamadryas) of Sukhumi, USSR. Am J Primatol 6:143-153.
32. Crawford MH, Devor EJ, O'Rourke DH, Yakovleva LA, Voevodin AF, Lapin B. 1987. Genetics of primate lymphomas in a baboon (Papio hamadryas) colony of Sukhumi, USSR. Genetica 73:145-157.
33. Crnokrak P, Roff DA. 1999. Inbreeding depression in the wild. Heredity 83:260-270.
34. De Ruiter JR, van Hooff JARAM, Scheffrhan W. 1994. Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129: 203-223.
35. Di Fiore A. 2003. Molecular genetic approaches to the study of primate behavior, social organization, and reproduction. Yearbook Phys Anthropol 46:62-99.
36. Dietz JM, Baker AJ. 1993. Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Anim Behav 46:1067-1078.
37. Dixson A. 2002. Sexual selection by cryptic female choice and the evolution of primate sexuality. Evol Anthropol 11(Suppl. 1): 195-199.
38. Dixson AF. 1998. Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press. 560p.
39. Eberle M, Kappeler PM. 2004. Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57:77-90.
40. Engelhardt A, Heistermann M, Hodges JK, Nuernberg P, Niemitz C. 2006. Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)-male monopolization, female mate choice or post-copulatory mechanism? Behav Ecol Sociobiol 59:740-752.
41. Evans BJ, Supriatna J, Melnick DJ. 2001. Hybridization and population genetics of two macaque species in Sulawesi, Indonesia. Evolution 55:1686-1702.
42. Fisher RA. 1930. The genetical theory of natural selection. Oxford: Clarendon Press. 318p.
43. Frankham R. 1995. Inbreeding and extinction: a threshold effect. Conserv Biol 9:792-799.
44. Frankham R. 2003. Genetics and conservation biology. CR Biol 326:S22-S29.
45. Frankham R, Ballou JD, Briscoe DA. 2002. Introduction to conservation genetics. Cambridge: Cambridge University Press. 617p.
46. Fredsted T, Pertoldi C, Olesen JM, Eberle M, Kappeler PM. 2004. Microgeographic heterogeneity in spatial distribution and mtDNA variability of gray mouse lemurs (Microcebus murinus, Primates: Cheirogaleidae). Behav Ecol Sociobiol 56:393-403.
47. Gallardo JA, Garcia X, Lhorente JP, Neira R. 2004. Inbreeding and inbreeding depression of female reproductive traits in two populations of Coho salmon selected using BLUP predictors of breeding values. Aquaculture 234:111-122.
48. Goossens B, Chikhi L, Ancrenaz M, Lackman-Ancrenaz I, Andau P, Bruford MW. 2006. Genetic signature of anthropogenic population collapse in orang-utans. Plos Biol 4: 285-291.
49. Gust DA, McCaster T, Gordon TP, Gergits WF, Casna NJ, Mc Clure HM. 1998. Paternity in sooty mangabeys. Int J Primatol 19: 83-94.
50. Hartl DL, Clark AG. 1997. Principles of population genetics. Sunderland: Sinauer Associates. 542p.
51. Hoffman JI, Boyd IL, Amos W. 2004. Exploring the relationship between parental relatedness and male reproductive success in the antartic fur seal Arctocephalus gazella. Evolution 58:2087-2099.
52. Inoue M, Mitsunaga F, Nozaki M, Ohsawa H, Takenaka A, Sugiyama Y, Shimizu K, Takenaka O. 1993. Male-dominance rank and reproductive success in an enclosed group of Japanese macaques - with special reference to post-conception mating. Primates 34:503-511.
53. Isachenko EF, Nayudu PL, Isachenko VV, Nawroth F, Michelmann HW. 2002. Congenitally caused fused labia in the common marmoset (Callithrix jacchus). J Med Primatol 31:350-355.
54. Keller LF, Waller DM. 2002. Inbreeding effects in wild populations. Trends Ecol Evol 17:230-241.
55. Kuester J, Paul A. 1992. Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120: 192-217.
56. Kuester J, Paul A, Arnemann J. 1994. Kinship, familiarity and mating avoidance in Barbary macaques, Macaca sylvanus. Anim Behav 48:1183-1194.
57. Lacy RC, Petric A, Warneke M. 1993. Inbreeding and outbreeding in captive populations of wild animal species. In: Thornhill NW, editor. The natural history of inbreeding and outbreeding. Chicago: University of Chicago Press. p 352-374.
58. Mandal A, Pant KP, Rout PK, Roy R. 2004. Effects of inbreeding on lamb survival in a flock of Muzaffarnagari sheep. Asian Austr J Anim 17:594-597.
59. Marshall TC, Coltman DW, Pemberton JM, Slate J, Spalton JA, Guinness FE, Smith JA, Pilkington JG, Clutton-Brock TH. 2002. Estimating the prevalence of inbreeding from incomplete pedigrees. Proc Roy Soc Lond B: Biol Sci 269:1533-1539.
60. Martin RD, Dixson AF, Wickings EJ. 1992. Paternity in primates: genetic tests and theories. Implications of human DNA fingerprinting. Basel: Karger. 288p.
61. Nakamichi M, Nobuhara H, Nobuhara T, Nakahashi M, Nigi H. 1997. Birth rate and mortality rate of infants with congenital malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata). Am J Primatol 42: 225-234.
62. Newman D, Pilson D. 1997. Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354-362.
63. Noble SJ, Chesser RK, Ryder OA. 1990. Inbreeding effects in captive populations of Ruffed Lemurs. Hum Evol 5:283-291.
64. Ohsawa H, Inoue M, Takenaka O. 1993. Mating strategy and reproductive success of male pata monkeys (Erythrocebus patas). Primates 34:533-544.
65. Packer C. 1979. Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim Behav 27:1-36.
66. Paul A, Kuester J, Timme A, Arnemann J. 1993. The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 34:491-502.
67. Peer K, Taborskyi M. 2005. Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sibling mating. Evolution 59:317-323.
68. Pemberton J. 2004. Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613-615.
69. Perrin N, Mazalov V. 1999. Dispersal and inbreeding avoidance. Am Nat 154:282-292.
70. Perrin N, Mazalov V. 2000. Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116-127.
71. Prugnolle F, Choisy M, Théron A, Durand P, De Meeus T. 2004. Sex-specific correlation between heterozygosity and clone size in a trematode Schistosoma mansoni. Mol Ecol 13:2859-2864.
72. Pujolar JM, Maes GE, Vancoillie C, Volckaert FAM. 2005. Growth rate correlates to individual heterozygosity in the European eel Anguilla anguilla L. Evolution 59:189-199.
73. Pusey A. 1990. Mechanisms of inbreeding avoidance in nonhuman primates. In: Feierman JR, editor. Pedophilia. NewYork: Springer. p 201-220.
74. Pusey AE, Packer C. 1987. Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: The University of Chicago Press. p 250-266.
75. Pusey A, Wolf M. 1996. Inbreeding avoidance in animals. Trends Ecol Evol 11:201-206.
76. Quinn TW, Quinn JS, Cooke F, White BN. 1987. DNA marker analysis detects multiple paternity and maternity in single broods of the lesser snow goose. Nature 326:392-394.
77. Ralls K, Ballou J. 1982. Effects of inbreeding on infant mortality in captive primates. Int J Primatol 3:491-505.
78. Ralls K, Harvey PH, Lyles AM. 1986. Inbreeding in natural populations of birds and mammals. In: Soulé ME, editor. Conservation biology - the science of scarcity and diversity. Sunderland, MA: Sinauer Associates. p 35-56.
79. Rawlins RG, Kessler MJ. 1983. Congenital and hereditary anomalies in the rhesus monkeys (Macaca mulatta) of Cayo Santiago. Teratology 28:169-174.
80. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491-494.
81. Schülke O, Kappeler PM, Zischler H. 2004. Small tested size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behav Ecol Sociobiol 55:293-301.
82. Seddon N, Amos W, Mulder RA, Tobias JA. 2004. Male heterozygosity predicts territory size song structure and reproductive success in a cooperatively breeding bird. Proc Roy Soc Lond B: Biol Sci 271: 1823-1829.
83. Setchell JM, Charpentier M, Wickings EJ. 2005. Sexual selection, age specific reproductive output and reproductive careers in mandrills (Mandrillus sphinx). Behav Ecol Sociobiol 58:474-485.
84. Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH. 2000. Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc Roy Soc Lond B: Biol Sci 267: 1657-1662.
85. Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC. 2004. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255-265.
86. Smith DG. 1986. Incidence and consequences of inbreeding in three captive groups of rhesus macaques (Macaca mulatta). In: Benirschke I, editor. Primates. The road to self-sustaining populations. New York: Springer-Verlag. p 857-874.
87. Smith DG. 1995. Absence of deleterious effects of inbreeding in rhesus macaques. Int J Primatol 16:855-870.
88. Soltis J, Thomsen R, Takenaka O. 2001. The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62: 485-494.
89. Stern BR, Smith DG. 1984. Sexual behaviour and paternity in three captive groups of rhesus monkeys (Macaca mulatta). Anim Behav 32:23-32.
90. Stills HF, Bullock BC. 1981. Congenital defects of squirrel monkeys (Saimiri sciureus). Vet Pathol 18:29-36.
91. Thünken T, Bakker TCM, Baldauf SA, Kullmann H. 2007. Active inbreeding in a cichlid fish and its adaptive significance. Curr Biol 17:225-229.
92. van Oosterhout C. Zijlstra WG, van Heuven MK, Brakefield PM. 2000. Inbreeding depression and genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Evolution 54:218-225.
93. Waller DM. 1993. The statics and dynamics of mating system evolution. In: Thornhill N, editor. The natural history of inbreeding and outbreeding. Chicago: University of Chicago Press. p 97-117.
94. Wang J. 2000. Effects of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutations. Genet Res Camb 76: 75-86.
95. Wetton JH, Carter RE, Parkin DT, Walters D. 1987. Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147-149.
96. Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M. 2004. A longitudinal analysis of reproductive skew in male rhesus macaques. Proc Roy Soc Lond B: Biol Sci 271:819-826.
97. Willis JH. 2000. The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53:1678-1691.
98. Wrege PH, Emlen ST. 1987. Biochemical determination of paternal uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153-160.