Kinship and social bonds in female chimpanzees (Pan troglodytes)

American Journal of Primatology

Volumn 71, Issue 10, 2009, Pages 840-851

  Langergraber, Kevin ^a   Mitani, John ^b   Vigilant, Linda ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPARATIVE STUDY; DISPERSAL; GROOMING; INTRASEXUAL INTERACTION; KINSHIP; MIGRATION; PRIMATE; SOCIAL BEHAVIOR; SPACE USE; TERRITORY;

ANIMAL; ARTICLE; FAMILY; FEMALE; MALE; PAN TROGLODYTES; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SOCIAL DISTANCE;

ANIMALS; FAMILY; FEMALE; MALE; PAN TROGLODYTES; SOCIAL DISTANCE;

MAMMALIA; PAN; PAN TROGLODYTES;

EID: 70349515197     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20711     Document Type: Article

References (112)

1. Altmann J. 1979. Age cohorts as paternal sibships. Behav Ecol Sociobiol 6:161-164.
2. 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 Lond B Biol Sci 273:513-522.
3. Aukett R, Ritchie J, Mill K. 1988. Gender differences in friendship patterns. Sex Roles 19:57-66.
4. Barth RJ, Kinder BN. 1988. A theoretical-analysis of sex-differnces in same-sex friendships. Sex Roles 19:349-363.
5. Bastani S. 2009. Family comes first: men's and women's personal networks in Tehran. Soc Netw 29:357-374.
6. Baumeister RF, Sommer KL. 1997. What do men want? Gender differences and two spheres of belongingness: comment on Cross and Madson (1997). Psychol Bull 122: 38-44.
7. Boesch C, Boesch-Achermann H. 2000. The Chimpanzees of the Tai Forest. Oxford: Oxford University Press.
8. Boesch C, Kohou G, Nene H, Vigilant L. 2006. Male competition and paternity in wild chimpanzees of the Tai forest. Am J Phys Anthropol 130:103-115.
9. Boinski S, Kauffman L, Ehmke E, Schet S, Vreedzam A. 2005. Dispersal patterns among three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis and S. sciureus): I. Divergent costs and benefits. Behaviour 142:525-632.
10. Bradley BJ, Doran-Sheehy DM, Vigilant L. 2007. Potential for female kin associations in wild western gorillas despite female dispersal. Proc R Soc Lond B Biol Sci 274:2179-2185.
11. Byrd-Craven J, Geary DC. 2007. Biological and evolutionary contributions to developmental sex differences. Reprod Biomed Online 15:12-22.
12. Cheney D, Seyfarth R. 1983. Nonrandom dispersal in free-ranging vervet monkeys: social and genetic consequences. Am Nat 122:392-412.
13. Cheney DL. 1992. Intragroup cohesion and intergroup hostility-the relation between grooming distributions and intergroup competition among female primates. Behav Ecol 3:334-345.
14. Clauset A, Newman MEJ, Moore C. 2004. Finding community structure in very large networks. Phys Rev E 70:066111.
15. Connor RC, Wells RS, Mann J, Read AJ. 2000. The bottlenose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H, editors. Cetacean Societies. Chicago: University of Chicago Press. p 91-126
16. Constable JL, Ashley MV, Goodall J, Pusey AE. 2001. Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279-1300.
17. Crockford C, Wittig RA, Whitten PL, Seyfarth RA, Cheney DL. 2008. Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53:254-265.
18. Croft DP, James R, Krause J. 2008. Exploring animal social networks. Princeton: Princeton University Press. 192p.
19. Di Bitetti MS. 2000. The distribution of grooming among female primates: testing hypotheses with the Shannon-Wiener diversity index. Behaviour 137:1517-1540.
20. Doncaster CP. 1990. Non-parametric estimates of interaction from radio-tracking data. J Theor Biol 143:431-443.
21. Dunbar RIM, Spoors M. 1995. Social networks, support cliques, and kinship. Hum Nat Interdiscip Biosoc Perspect 6:273-290.
22. Emery Thompson M, Kahlenberg SM, Gilby IC, Wrangham RW. 2007. Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park. Anim Behav 73:501-512.
23. Gabriel S, Gardner WL. 1999. Are there "his" and "hers" types of interdependence? The implications of gender differences in collective versus relational interdependence for affect, behavior, and cognition. J Pers Soc Psychol 77:642-655.
24. Geary DC. 2006. Sex differences in social behavior and cognition: Utility of sexual selection for hypothesis generation. Horm Behav 49:273-275.
25. Gero S, Engelhaupt D, Whitehead H. 2008. Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness. Behav Ecol Sociobiol 63:143-151.
26. Gilby IC, Wrangham R. 2008. Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behav Ecol Sociobiol 62:1831-1842.
27. Goldberg TL, Wrangham RW. 1997. Genetic correlates of social behaviour in wild chimpanzees: evidence from mitochondrial DNA. Anim Behav 54:559-570.
28. Goodnight KF, Queller DC. 1999. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231-1234.
29. Guimera R, Sales-Pardo M, Amaral LAN. 2004. Modularity from fluctuations in random graphs and complex networks. Phys Rev E 70:025101.
30. Halperin S. 1979. Temporary association patterns in free ranging chimpanzees: an assessment of individual grouping preferences. In: Hamburg D, McCown E, editors. The great apes. Menlo Park: Benjamin/Cummings. p 491-499.
31. Hamilton WD. 1963. The evolution of altruistic behavior. Am Nat 97:354-356.
32. Hamilton WD. 1964a. The genetical evolution of social behaviour. I. J Theor Biol 7:1-16.
33. Hamilton WD. 1964b. The genetical gvolution of social behaviour. II. J Theor Biol 7:17-52.
34. Hasegawa T. 1990. Sex differences in ranging patterns. In: Nishida T, editor. The Chimpanzees of the Mahale Mountains: sexual and life history strategies. Tokyo: University of Tokyo Press. p 99-114.
35. Heinsohn R, Dunn P, Legge S, Double M. 2000. Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs. Proc R Soc Lond B Biol Sci 267:243-249.
36. Hemelrijk CK. 1990. Models of, and tests for, reciprocity, unidirectionality and other social interaction patterns at a group level. Anim Behav 39:1013-1029.
37. Holekamp KE, Sakai ST, Lundrigan BL. 2007. Social intelligence in the spotted hyena (Crocuta crocuta). Philos Trans R Soc B Biol Sci 362:523-538.
38. Inoue E, Inoue-Murayama M, Vigilant L, Takenaka O, Nishida T. 2008. Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors. Am J Phys Anthropol 137:256-262.
39. Jack KM, Fedigan LM. 2004. Male dispersal patterns in whitefaced capuchins, Cebus capucinus. Part 1: patterns and causes of natal emigration. Anim Behav 67:761-769.
40. Kahlenberg SM, Thompson ME, Muller MN, Wrangham RW. 2008. Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Anim Behav 76:1497-1509.
41. Kawanaka K. 1984. Association, ranging, and the social unit in chimpanzees of the Mahale mountains, Tanzania. Int J Primatol 5:411-434.
42. Kawanaka K, Nishida T. 1974. Recent advances in the study of inter-unit-group relationships and social structure of wild chimpanzees of the Mahale Mountains. Symposium of the 5th Congress of the International Primatology Society. Nagoya, Japan. p 173-186.
43. Koenig WD, Hooge PN, Stanback MT, Haydock J. 2000. Natal dispersal in the cooperatively breeding acorn woodpecker. Condor 102:492-502.
44. Langergraber KE, Mitani JC, Vigilant L. 2007a. The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104:7786-7790.
45. Langergraber KE, Siedel H, Mitani JC, Wrangham RW, Reynolds V, Hunt KD, Vigilant L. 2007b. The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS One 10:e973.
46. Le Galliard J-F, Gundersen G, Andreassen HP, Stenseth NC. 2006. Natal dispersal, interactions among siblings and intrasexual competition. Behav Ecol 17:733-740.
47. Lehmann J, Boesch C. 2005. Bisexually bonded ranging in chimpanzees (Pan troglodytes verus). Behav Ecol Sociobiol 57:525-535.
48. Lehmann J, Boesch C. 2008. Sexual differences in chimpanzee sociality. Int J Primatol 29:65-81.
49. Lehmann J, Boesch C. 2009. Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Anim Behav 77:377-387.
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. Lusseau D, Schneider K, Boisseau OJ, Haase P, Slooten E, Dawson SM. 2003. The bottlenose dolphin community of Doubtful Sound features a large proportion of long-lasting associations-Can geographic isolation explain this unique trait? Behav Ecol Sociobiol 54:396-405.
52. Lusseau D, Whitehead H, Gero S. 2008. Incorporating uncertainty into the study of animal social networks. Anim Behav 75:1809-1815.
53. Lynch M, Ritland K. 1999. Estimation of pairwise relatedness with molecular markers. Genetics 152:1753-1766.
54. Markovits H, Benenson J, Dolenszky E. 2001. Evidence that children and adolescents have internal models of peer interactions that are gender differentiated. Child Dev 72:879-886.
55. Markovits H, Benenson J, White S. 2006. Gender and priming differences in speed of processing of information relating to social structure. J Exp Soc Psychol 42:662-667.
56. Marsden PV. 1987. Core discussion networks of Americans. Am Sociol Rev 52:122-131.
57. Matsumoto-Oda A. 1999. Mahale chimpanzees: grouping patterns and cycling females. Am J Primatol 47:197-207.
58. Meikle DB, Vessey SH. 1981. Nepotism among rhesus monkey brothers. Nature 29:160-161.
59. Mitani JC. 2006. Demographic influences on the behavior of chimpanzees. Primates 47:6-13.
60. Mitani JC. 2009. Male chimpanzees form enduring and equitable social bonds. Anim Behav 77:633-640.
61. Mitani JC, Merriwether DA, Zhang CB. 2000. Male affiliation, cooperation and kinship in wild chimpanzees. Anim Behav 59:885-893.
62. Mitani JC, Watts DP, Muller MN. 2002. Recent developments in the study of wild chimpanzee behavior. Evol Anthropol 11:9-25.
63. Moore G. 1990. Structural determinants of men's and women's social networks. Am Sociol Rev 55:726-735.
64. Muller M. 2002. Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant L, editors. Behavioral diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 112-124.
65. Muller MN, Mitani JC. 2005. Conflict and cooperation in wild chimpanzees. Adv study behav 35:275-331.
66. Murdoch GP. 1981. Atlas of World Cultures. Pittsburgh: University of Pittsburgh Press.
67. Murray CM, Eberly LE, Pusey AE. 2006. Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behav Ecol 17: 1020-1028.
68. Murray CM, Mane SV, Pusey AE. 2007. Dominance rank influences female space use in wild chimpanzees, Pan troglodytes: towards an ideal despotic distribution. Anim Behav 74:1795-1804.
69. Murray CM, Wroblewski E, Pusey A. 2008. New case of intragroup infanticide in the chimpanzees of Gombe National Park. Int J Primatol 28:23-37.
70. Newman MEJ. 2004. Analysis of weighted networks. Phys Rev E 70:9.
71. Newman MEJ. 2006. Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577-8582.
72. Nishida T. 1968. The social group of wild chimpanzees in the Mahale mountains. Primates 9:167-224.
73. Nishida T, Kawanaka K. 1972. Inter-unit-group relationships among wild chimpanzees of the Mahale mountains. Kyoto Univ Afr Stud 7:131-169.
74. Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K. 2003. Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59: 99-121.
75. Packer C, Gilbert DA, Pusey AE, O'Brien SJ. 1991. A molecular genetic analysis of kinship and cooperation in African lions. Nature 351:562-565.
76. Pepper JW, Mitani JC, Watts DP. 1999. General gregariousness and specific social preferences among wild chimpanzees. Int J Primatol 20:613-632.
77. Perrin N, Goudet J. 2001. Inbreeding, kinship, and the evolution of natal dispersal. In: Clobert J, Danchin E, Dhondt AE, Nichols JD, editors. Dispersal. Oxford: Oxford University Press. p 123-142.
78. Perrin N, Lehmann L. 2001. Is dispersal driven by the costs of dispersal or the benefits of philopatry? A role for kin discrimination mechanisms. Am Nat 158:471-483.
79. Pusey AE, Williams J. 1997. The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828-831.
80. Rodseth L, Novak SA. 2006. The impact of primatology on the study of human society. In: Barkow JH, editor. Missing the revolution: darwinism for social scientists. New York: Oxford University Press. p 187-220.
81. Seeley EA, Gardner WL, Pennington G, Gabriel S. 2003. Circle of friends or members of a group? Sex differences in relational and collective attachment to groups. Group Processes Intergroup Relat 6:251-263.
82. Sharp SP, Baker MB, Hadfield JD, Simeoni M, Hatchwell BJ. 2008a. Natal dispersal and recruitment in a cooperatively breeding bird. Oikos 117:1371-1379.
83. Sharp SP, Simeoni M, Hatchwell BJ. 2008b. Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird. Proc R Soc Lond B Biol Sci 275:2125-2130.
84. Silk JB. 2003. Cooperation without counting: the puzzle of friendship. In: Hammerstein P, editor. The genetic and cultural evolution of cooperation. Cambridge: The MIT Press. p 37-54.
85. Silk JB. 2006. Practicing hamilton's rule: kin selection in primate groups. In: Kappeler PM, van Schaik CP, editors. Cooperation in primates and humans. Berlin: Springer. p 25-46.
86. Silk JB. 2007a. The adaptive value of sociality in mammalian groups. Philos Trans R Soc Lond B Biol Sci 362:539-559.
87. Silk JB. 2007b. Social components of fitness in primate groups. Science 317:1347-1351.
88. Silk JB, Alberts SC, Altmann J. 2003. Social bonds of female baboons enhance infant survival. Science 302:1231-1234.
89. 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.
90. 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.
91. Sterck EHM, Watts DP, vanSchaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291-309.
92. Struhsaker TT. 1997. Ecology of an African rainforest. Gainsville: University Press of Florida. 434p.
93. Sugiyama Y. 2004. Demographic parameters and life history of chimpanzees at Bossou, Guinea. Am J Phys Anthropol 124:154-165.
94. Taylor SE, Cousino Klein L, Lewis BP, Gruenewald TL, Gurung RAR, Updegraff JA. 2000. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 107:411-429.
95. Townsend SW, Slocombe KE, Thompson ME, Zuberbuhler K. 2007. Female-led infanticide in wild chimpanzees. Curr Biol 17:R355-R356.
96. van Hoof JARAM. 2000. Relationships among non-human primate males: a deductive framework. In: Kappeler P, editor. Primate males. Cambridge: Cambridge University Press. p 183-191.
97. van Schaik CP. 1989. The ecology of social relationships amongst female primates. In: Standon V, Foley RA, editors. Comparative socioecology: the behavioural ecology of humans and other mammals. Oxford: Blackwell Scientific Publications. p 195-218.
98. Vigil JM. 2007. Asymmetries in the friendship preferences and social styles of men and women. Hum Nat Interdiscip Biosoc Perspect 18:143-161.
99. Vigilant L, Hofreiter M, Siedel H, Boesch C. 2001. Paternity and relatedness in wild chimpanzee communities. Proceedings of the National Academy of Sciences of the United States of America 98:12890-12895.
100. Wakefield ML. 2008. Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. Int J Primatol 29: 907-929.
101. Widdig A, Nurnberg P, Krawczak M, Streich WJ, Bercovitch F. 2001. Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc Natl Acad Sci USA 98:13769-13773.
102. Widdig A, Nurnberg P, Krawczak M, Streich WJ, Bercovitch F. 2002. Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139:371-391.
103. Wilkins JF, Marlowe FW. 2005. Sex-biased migration in humans: what should we expect from genetic data? BioEssays 28:290-300.
104. Williams JM, Liu HY, Pusey AE. 2002a. Costs and benefits of grouping for female chimpanzees at Gombe. In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. p 192-203.
105. Williams JM, Pusey AE, Carlis JV, Farm BP, Goodall J. 2002b. Female competition and male territorial behaviour influence female chimpanzees' ranging patterns. Anim Behav 63:347-360.
106. Williams JM, Oehlert G, Pusey AE. 2004. Why do male chimpanzees defend a group range? Anim Behav 68: 523-532.
107. Wilson M, Wrangham RW. 2003. Intergroup relationships in chimpanzees. Annu Rev Anthropol 32:363-392
108. Wittig RA, Crockford C, Lehmann J, Whitten PL, Seyfarth RM, Cheney DL. 2008. Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54: 170-177.
109. Wrangham R, Smuts BB. 1980. Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil Suppl 28:13-31.
110. Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75:262-300.
111. Wrangham RW, Wilson ML, Muller MN. 2004. Comparative rates of violence in chimpanzees and humans. Primates 47:14-26.
112. Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, Pusey AE. 2009. Male dominance rank and reproductive success in chimpanzees, Pan troglo-dytes schweinfurthii. Anim Behav.