Patterns of paternity and group fission in wild multimale mountain gorilla groups

American Journal of Physical Anthropology

Volumn 135, Issue 3, 2008, Pages 263-274

  Nsubuga, Anthony M ^a,b   Robbins, Martha M ^a   Boesch, Christophe ^a   Vigilant, Linda ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b ZOOLOGICAL SOCIETY OF SAN DIEGO   (United States)

Author keywords

Beringei; Bwindi; Microsatellite genotyping; Mutation; Reproductive skew; Uganda

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; FECES ANALYSIS; GENOTYPE; GORILLA; MALE; MOUNTAIN GORILLA; NATIONAL PARK; NONHUMAN; PATERNITY; PROGENY; REPRODUCTIVE SUCCESS; SOCIETY; UGANDA;

ANIMALS; ANIMALS, WILD; DNA FINGERPRINTING; FEMALE; GEOGRAPHY; GORILLA GORILLA; MALE; PATERNITY; SOCIAL DOMINANCE; UGANDA;

EID: 39049105224     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.20740     Document Type: Article

References (101)

1. Alberts SC. 1999. Paternal kin discrimination in wild baboons. Proc R Soc Lond B Biol Sci 266:1501-1506.
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. Alberts SC, Watts HW, Altmann J. 2003. Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821-840.
5. Archie EA, Moss CJ, Alberts SC. 2006. The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc B 273:513-522.
6. Baker RR, Bellis MA. 1993. Human sperm competition: ejaculate manipulation by females and a function for the female orgasm. Anim Behav 46:887-909.
7. Birkhead TR. 1998. Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:1212-1218.
8. Boesch C, Kohou G, Néné H, and Vigilant L. 2006. Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130:103-115.
9. Bradley BJ, Boesch C, Vigilant L. 2000. Identification and redesign of human microsatellite markers for genotyping wild chimpanzee (Pan troglodytes verus) and gorilla (Gorilla gorilla gorilla) DNA from faeces. Conserv Genet 1:289-292.
10. Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L. 2004. Dispersed male networks in western gorillas. Curr Biol 14:510-513.
11. Bradley BJ, Robbins MM, Williamson EA, Steklis DH, Steklis NG, Eckhardt N, Boesch C, Vigilant L. 2005. Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102:9418-9423.
12. Bradley BJ, Vigilant L. 2002. False alleles derived from microbial DNA probe pose a potential source of error in microsatellite genotyping of DNA from faeces. Mol Ecol Notes 2:602-605.
13. Brinkmann B, Klintschar M, Neuhuber F, Huhne J, Rolf B. 1998. Mutation rate in human microsatellites: influence of the structure and length of tandem repeat. Am J Hum Genet 62:1408-1415.
14. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179-181.
15. Campbell P, Schneider CJ, Adnan AM, Zubaid A, Kunz TH. 2006. Comparative population structure of Cynopterus fruit bats in peninsular Malaysia and southern Thailand. Mol Ecol 15:29-47.
16. Chakraborty R, Meagher TR, Smouse PE. 1988. Parentage analysis with genetic markers in natural populations. I. The expected proportion of offspring with unambiguous paternity. Genetics 118:527-536.
17. Clifford SL, Jeffrey K, Bruford MW, Wickings EJ. 1999. Identification of polymorphic microsatellite loci in the gorilla (Gorilla gorilla gorilla) using human primers: application to noninvasively collected samples. Mol Ecol 8:1551-1561.
18. Clutton-Brock TH. 1989a. Female transfer and inbreeding avoidance in social mammals. Nature 337:70-72.
19. Clutton-Brock TH. 1989b. Mammalian mating systems. Proc R Soc Lond B Biol Sci 236:339-372.
20. Constable JL, Ashley MV, Goodall J, Pusey AE. 2001. Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279-1300.
21. Davies NB, Hartley IR. 1996. Food patchness, territory overlap and social sysytems: an experiment with dunnocks, Prunella mondularis. J Anim Ecol 65:837-846.
22. Fiore A. 2003. Molecular genetic approaches to the study of primate behavior, social organisation, and reproduction. Yrbk Phys Anthropol 46:62-99.
23. Eberhard WG. 1998. Female control: sexual selection by cryptic female choice. Princeton: Princeton University Press.
24. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
25. Engelhardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C. 2006. Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis): male monopolisation, female mate choice or post-copulatory mechanisms. Behav Ecol Sociobiol 59:740-752.
26. Engh AL, Funk SM, van Horn RC, Scribner KT, Bruford MW, Libants S, Szykman M, Smale L, Holekamp KE. 2002. Reproductive skew among males in a female-dominated mammalian society. Behav Ecol 13:193-200.
27. Fernando P, Vidya TNC, Rajpakse A, Dangolla A, Melnick DJ. 2003. Reliable noninvasive genotyping: fantasy or reality? J Hered 94:115-123.
28. Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU. 2000. High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8-17.
29. Ganas J, Robbins MM. 2005. Ranging behaviour of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda: a test for ecological constraints model. Behav Ecol Sociobiol 58:277-288.
30. Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, McNeilage A. 2004. Dietary variability of mountain gorillas in Bwindi Impenetrable National Park. Uganda. Int J Primatol 25: 1043-1072.
31. Garnier JN, Bruford MW, Goossens B. 2001. Mating system and reproductive skew in the black rhinoceros. Mol Ecol 10:2031-2041.
32. Gatti S, Levréro F, Ménard N, Gautier-Hion A. 2004. Population and group structure of western lowland gorillas (Gorilla gorilla gorilla) at Lokoue, Republic of Congo. Am J Primatol 63:111-123.
33. Goossens B, Chikhi L, Utami SS, Ruiter J, Bruford MW. 2000. A multi-samples, multi-extracts approach for microsatellites analysis of faecal samples in an arboreal ape. Conserv Genet 1:157-162.
34. Goossens B, Graziani L, Waits LP, Farand E, Magnolon S, Coulon J, Bel M-C, Taberlet P, Allainé D. 1998. Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behav Ecol Sociobiol 43:281-288.
35. Griffin SC, Owens IPF, Thuman KA. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function Mol Ecol 11:2195-2212.
36. Harcourt AH. 1978. Strategies of emigration and transfer by primates, with particular reference to gorillas. Z Tierpsychol 48:401-420.
37. Ibarguchi G, Gissing GJ, Gaston AJ, Boag PT, Friesen VL. 2004. Male-biased mutation rates and the overestimation of extra-pair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia. Alcidae). J Hered 95:209-216.
38. Jones AG, Ardren WR. 2003. Methods of parentage analysis in natural populations. Mol Ecol 12:2511-2523.
39. Jones AG, Avise JC. 2001. Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity. J Hered 92:150-158.
40. Jones AG, Rosenqvist G, Berglund A, Avise JC. 1999. Clustered microsatellite mutation in the pipefish (Syngnathus typhle). Genetics 152:1057-1063.
41. Kalpers J, Williamson EA, Robbins MM, McNeilage A, Nzamurambaho A, Ndakasi L, Mugiri G. 2003. Gorillas in the crossfire: assessment of population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37:326-337.
42. Kappeler PM. 2000. Causes and consequences of unusual sex ratios among lemurs. In: Kappeler PM, editor. Primate males. Cambridge: Cambridge University Press. p 3-7.
43. Kappeler PM, van Schaik CP. 2002. Evolution of primate social systems. Int J Primatol 23:707-740.
44. Kokko H, Brooks R, Jennions MD, Morley J. 2003. The evolution of mate choice and mating biases. Proc R Soc Lond B 270:653-664.
45. Langergraber KE, Mitani JC, and Vigilant L. 2007. The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104:7786-7790.
46. Lefebvre D, Ménard N, Pierre JS. 2003. Modelling the influence of demographic parameters on group structure in social species with dispersal asymmetry and group fission. Behav Ecol Sociobiol 53:402-410.
47. Lehmann J, Fickenscher G, Boesch C. 2006. Kin biased investment in wild chimpanzees. Behaviour 143:931-955.
48. Lindenfors P, Fröberg L, Nunn C. 2004. Females drive primate social evolution. Proc R Soc Lond B (Suppl) Biol Lett 271: S101-S103.
49. Linklater WL. 2000. Adaptive explanation in socio-ecology: lessons from the Equidae. Biol Rev 75:1-20.
50. Lukas D, Reynolds V, Boesch C, Vigilant L. 2005. To what extent does living in a group mean living with kin? Mol Ecol 14:2181-2196.
51. MacKiewicz M, Fletcher DE, Wilkins SD, Dewoody JA, Avise JC. 2002. A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Mol Ecol 11:1877-1883.
52. Marshall TC, Slate J, Kruuk LE, Pemberton JM. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639-655.
53. McNeilage A, Robbins MM, Gray M, Olupot W, Babaasa D, Bitariho R, Kasangaki A, Rainer H, Asuma S, Mugiri G, Baker J. 2006. Census of the mountain gorilla (Gorilla beringei beringei) population in Bwindi Impenetrable National Park, Uganda. Oryx 40:419-427.
54. Melnick DJ, Kidd KK. 1983. The genetic consequences of social group fission in a wild population of rhesus monkeys (Macaca mulatta). Behav Ecol Sociobiol 12:229-236.
55. Ménard N, Vallet D. 1993. Dynamics of fission in a wild Barbary macaques group (Macaca sylvanus). Int J Primatol 14:479-500.
56. Mitani JC, Gros-Louis J, Manson JH. 1996. Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38:315-332.
57. Möller LM, Beheregaray LB. 2004. Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Mol Ecol 13:1607-1612.
58. Morin PA, Chambers KE, Boesch C, Vigilant L. 2001. Quantitative PCR analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzes (Pan troglodytes verus). Mol Ecol 10:1835-1844.
59. Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, Vigilant L. 2006. Father-daughter inbreeding avoidance in a wild primate population. Curr Biol 16:156-157.
60. Nsubuga AM, Robbins MM, Roeder AD, Morin AP, Boesch C, Vigilant L. 2004. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 13:2089-2094.
61. Nunn C. 1999. The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1-13.
62. Paetkau D, Strobeck C. 1994. Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489-495.
63. Parnell RJ. 2002. Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. Am J Primatol 56:193-206.
64. Paul A. 2002. Sexual selection and mate choice. Int J Primatol 23:877-904.
65. Piggott MP. 2004. Effect of sample age and season of collection on the reliability of microsatellite genotyping of faecal DNA. Wildlife Res 31:485-493.
66. Raymond M, Rousset F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248-249.
67. Robbins AM, Robbins MM. 2005. Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 58:295-309.
68. Robbins MM. 1995. A demographic analysis of male life history and social structure of mountain gorilla groups. Behaviour 132:255-299.
69. Robbins MM. 1999. Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013-1020.
70. Robbins MM. 2001. Variation in the social system of mountain gorillas: the male perspective. In: Robbins MM, Sicotte P, Stewart K, editors. Mountain gorillas: three decades of research at Karisoke. Cambridge: Cambridge University Press, p 30-58.
71. Robbins MM. 2007. Gorillas: diversity in ecology and behaviour. In: Campbell CJ, Fuentes A, Panger M, Mackinnon KC, Bearder S, editors. Primates in perspective. Oxford: Oxford University Press. p 305-321.
72. Robbins MM, Bermejo M, Cipolletta C, Magliocca F, Parnell J, Stokes E. 2004. Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol 64:145-159.
73. Roon DA, Waits LP, Kendall KC. 2005. A simulation test of the effectiveness of several methods for error-checking non-invasive genetic data. Anim Conserv 8:203-215.
74. Roosen-Runge EC. 1977. The process of spermatogesis in animals. Cambridge: Cambridge University Press.
75. Sajantila A, Lukka M, Syvanen AC. 1999. Experimentally observed germline mutations at human micro- and minisatellite loci. Euro J Hum Genet 7:263-266.
76. Setchell JM, Charpentier M, Wickings E. 2005. Mate guarding and paternity in mandrills: factors influencing α male monopoly. Anim Behav 70:1105-1120.
77. Silk JB, Altmann J, Alberts SC. 2006a. Social relationships among adult female baboons (Papio cynocephalus). I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61: 183-195.
78. Silk JB, Altmann J, Alberts SC. 2006b. Social relationships among adult female baboons (Papio cynocephalus). II. Variation in the quality and stability of social bonds. Behav Ecol Sociobiol 61:197-204.
79. Smith K. 2000. Paternal kin matter: the distribution of social behavior among wild, adult females baboons. Ph.D. thesis, University of Chicago, Chicago.
80. Smith KL, Alberts SC, Altmann J. 2003. Wild female baboons bias their social behaviour towards paternal half-sisters. Proc R Soc Lond B Sci 270:503-510.
81. Sterck EHM, Watts DP, van Schaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291-309.
82. Stokes E, Richard J, Parnell J, Olejniczak C. 2003. Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav Ecol Sociobiol 54:329-339.
83. Strier K. 2004. The impact of patrilineal kinship behaviour. In: Chapais B, Berman CM, editors. Kinship and behaviour in primates. Oxford: University of Oxford. p 177-199.
84. Stumpf R, Boesch C. 2006. The efficacy of female choice in chimpanzees of the Taï Forest, Côte d'Ivoire. Behav Ecol Sociobiol 60:749-765.
85. Stumpf RM, Boesch C. 2005. Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire. Behav Ecol Sociobiol 57:511-524.
86. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J. 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189-3194.
87. Taberlet P, Waits LP, Luikart G. 1999. Noninvasive genetics sampling: look before you leap. Trends Ecol Evol 14:323-327.
88. van Noordwijk MA, and Van Schaik CP. 2004. Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates: a comparative perspective. Cambridge: Cambridge University Press. p 208-229.
89. van Schaik CP, Kappeler PM. 1997. Infanticide risk and the evolution of male-female association in primates. Proc R Soc Lond B Sci 264:1687-1694.
90. Vigilant L, Hofreiter M, Siedel H, Boesch C. 2001. Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci USA 98:12890-12895.
91. Wahaj SA, van Horn RC, van Horn TL, Dreyer R, Hilgris R, Swarz J, Holekamp KE. 2004. Kin discrimination in spotted hyena (Crocuta crocuta): nepotism among siblings. Behav Ecol Sociobiol 56:237-247.
92. Watts DP. 1989. Infanticide in mountain gorillas: new cases and consideration of evidence. Ethology 81:1-18.
93. Watts DP. 1991. Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211-225.
94. Watts DP. 2000. Causes and consequences of variation in male mountain gorilla life histories and group membership. In: Kappeler PM, editor. Primate males. Cambridge: Cambridge University Press. p 169-180.
95. Watts DP. 2003. Gorilla social relationships: a comparative review. In: Taylor AB, Goldsmith ML, editors. Gorilla biology: a multidisciplinary perspective. Cambridge (England): Cambridge University Press. p 302-327.
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 R Soc Lond B 271:819-826.
97. Widdig A, Jürgen W, Nürnberg P, Croucher PJP, Bercovitch FB, Krawczak M. 2006a. Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behav Ecol Sociobiol 61:205-214.
98. Widdig A, Nürnberg P, Bercovitch FB, Trefilov A, Berard JB, Kessler MJ, Schmidtke J, Streich WJ, Krawczak M. 2006b. Consequences of group fission for the patterns of relatedness among rhesus macaques. Mol Ecol 15:3825-3832.
99. Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB. 2001. Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc Natl Acad Sci USA 98:13769-13773.
100. Wimmer B, Kappeler PM. 2002. The effects of sexual selection and life history on the genetic structure of red-fronted lemur, Eulemur fulvus rufus, groups. Anim Behav 64:557-568.
101. Woodruff RC, Thompson JN. 1992. Have premeiotic clusters of mutations been overlooked in evolutionary theory? J Evol Biol 5:457-464.