The socio-genetics of a complex society: Female gelada relatedness patterns mirror association patterns in a multilevel society

Molecular Ecology

Volumn 23, Issue 24, 2014, Pages 6179-6191

  Snyder Mackler, Noah ^a   Alberts, Susan C ^a,b   Bergman, Thore J ^c  

^a DUKE UNIVERSITY   (United States)

^b INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

fission; gelada; genetic structure; multilevel society

Indexed keywords

ANIMALIA; CERCOPITHECIDAE; THEROPITHECUS GELADA;

MITOCHONDRIAL DNA;

ANIMAL; ANIMAL BEHAVIOR; FEMALE; GENETICS; GENOTYPE; MALE; PHYSIOLOGY; REPRODUCTIVE FITNESS; SOCIAL BEHAVIOR; THEROPITHECUS;

ANIMALS; BEHAVIOR, ANIMAL; DNA, MITOCHONDRIAL; FEMALE; GENETIC FITNESS; GENOTYPE; MALE; SOCIAL BEHAVIOR; THEROPITHECUS;

EID: 84919740739     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12987     Document Type: Article

References (108)

1. Abegglen JJ, (1984) On Socialization in Hamadryas Baboons: A Field Study. Bucknell University Press, Lewisburg, Pennsylvania.
2. Alberts SC, Buchan JC, Altmann J, (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Animal Behaviour, 72, 1177-1196.
3. Alexander RD, (1974) The evolution of social behavior. Annual Review of Ecology and Systematics, 5, 325-383.
4. Altmann J, Alberts SC, Haines SA, et al,. (1996) Behavior predicts genetic structure in a wild primate group. Proceedings of the National Academy of Sciences, 93, 5797-5801.
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. Proceedings of the Royal Society of London B: Biological Sciences, 273, 513-522.
6. Archie EA, Maldonado JE, Hollister-Smith JA, et al,. (2008) Fine-scale population genetic structure in a fission-fusion society. Molecular Ecology, 17, 2666-2679.
7. Armitage KB, (1987) Social dynamics of mammals: reproductive success, kinship and individual fitness. Trends in Ecology & Evolution, 2, 279-284.
8. Armitage KB, Schwartz OA, (2000) Social enhancement of fitness in yellow-bellied marmots. Proceedings of the National Academy of Sciences, 97, 12149-12152.
9. Aureli F, Shaffner C, Boesch C, et al,. (2008) Fission-fusion dynamics: new research frameworks. Current Anthropology, 49, 627-654.
10. Beehner JC, Bergman TJ, (2008) Infant mortality following male takeovers in wild geladas. American Journal of Primatology, 70, 1152-1159.
11. Belay G, Mori A, (2006) Intraspecific phylogeographic mitochondrial DNA (D-loop) variation of gelada baboon, Theropithecus gelada, in Ethiopia. Biochemical Systematics and Ecology, 34, 554-561.
12. Belay G, Shotake T, (1998) Blood protein variation of a new population of gelada baboons (Theoropithecus gelada), in the Southern Rift Valley, Arsi Region, Ethiopia. Primates, 39, 183-198.
13. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM, (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology & Evolution, 16, 314-321.
14. Bergl R, Vigilant L, (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Molecular Ecology, 16, 501-516.
15. Bradley BJ, Doran-Sheehy DM, Vigilant L, (2007) Potential for female kin associations in wild western gorillas despite female dispersal. Proceedings of the Royal Society of London B: Biological Sciences, 274, 2179-2185.
16. Buchan JC, Alberts SC, Silk JB, Altmann J, (2003) True paternal care in a multi-male primate society. Nature, 425, 179-181.
17. Chapais B, Gauthier C, Prud'Homme J, Vasey P, (1997) Relatedness threshold for nepotism in Japanese macaques. Animal Behaviour, 53, 1089-1101.
18. Chapais B, Savard L, Gauthier C, (2001) Kin selection and the distribution of altruism in relation to degree of kinship in Japanese macaques (Macaca fuscata). Behavioral Ecology and Sociobiology, 49, 493-502.
19. Colmenares F, (1992) Clans and harems in a colony of hamadryas and hybrid baboons: male kinship, familiarity and the formation of brother-teams. Behaviour, 121, 61-94.
20. Connor R, Wells R, Mann J, Read A, (2000) The bottlenose dolphin. In: Cetacean Societies (eds, Mann J, Conno RC, Tyack PL, Whitehead H,), pp. 91-126. University of Chicago Press, Chicago, Illinois.
21. Cords M, Rowell T, (1986) Group fission in blue monkeys of the Kakamega Forest, Kenya. Folia Primatologica, 46, 70-82.
22. Coulon A, Guillot G, Cosson JF, et al,. (2006) Genetic structure is influenced by landscape features: empirical evidence from a roe deer population. Molecular Ecology, 15, 1669-1679.
23. Cresswell W, (1994) Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Animal Behaviour, 47, 433-442.
24. De Vos A, O'Riain MJ, (2010) Sharks shape the geometry of a selfish seal herd: experimental evidence from seal decoys. Biology Letters, 6, 48-50.
25. Di Fiore A, (2012) Genetic consequences of primate social organization. In: The Evolution of Primate Societies (eds, Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB,), pp. 269-292. University of Chicago Press, Chicago, Illinois.
26. Dunbar RIM, (1983) Structure of gelada baboon reproductive units. II. Social relationships between reproductive females. Animal Behaviour, 31, 556-564.
27. Dunbar RIM, (1984) Reproductive Decisions: An Economic Analysis of Gelada Baboon Social Strategies. Princeton University Press, Princeton, New Jersey.
28. Dunbar RIM, (1986) The social ecology of gelada baboons. In: Ecological Aspects of Social Evolution (eds., Rubenstein DI, Wrangham RW,), pp. 332-351. Princeton University Press, Princeton, New Jersey.
29. Dunbar RIM, (1989) Reproductive strategies of female gelada baboons. In: The Sociobiology of Sexual and Reproductive Strategies (eds, Rasa A, Vogel C, Voland E,), pp. 74-92. Chapman & Hall, London, UK.
30. Dunbar RIM, (1993) Social organization of the gelada. In: Theropithecus: The Rise and Fall of a Genus (ed., Jablonski NG,), pp. 425-439. University Press, Cambridge.
31. Dunbar RIM, Dunbar EP, (1975) Social dynamics of gelada baboons. In: Contributions to Primatology (eds, Kuhn H, Luckett WP, Noback CR, Schultz AH, Starck D, Szalay FS,), pp. 1-157. S. Karger, Basel.
32. Eriksson J, Siedel H, Lukas D, et al,. (2006) Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Molecular Ecology, 15, 939-949.
33. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE a simulation study. Molecular Ecology, 14, 2611-2620.
34. Excoffier L, Lischer HEL, (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
35. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
36. Frère CH, Krützen M, Mann J, et al,. (2010) Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins. Animal Behaviour, 80, 481-486.
37. Greenwood P, (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28, 1140-1162.
38. Grüter CC, Chapais B, Zinner D, (2012) Evolution of multilevel social systems in nonhuman primates and humans. International Journal of Primatology, 33, 1002-1037.
39. Guschanski K, Caillaud D, Robbins MM, Vigilant L, (2008) Females shape the genetic structure of a gorilla population. Current Biology, 18, 1809-1814.
40. Hackländer K, Möstl E, Arnold W, (2003) Reproductive suppression in female Alpine marmots, Marmota marmota. Animal Behaviour, 65, 1133-1140.
41. Hamilton WD, (1964) The genetical evolution of social behaviour. Journal of Theoretical Biology, 7, 1-52.
42. Hamilton WD, (1971) Geometry for the selfish herd. Journal of Theoretical Biology, 31, 295-311.
43. Hapke A, Zinner D, Zischler H, (2001) Mitochondrial DNA variation in Eritrean hamadryas baboons (Papio hamadryas hamadryas): life history influences population genetic structure. Behavioral Ecology and Sociobiology, 50, 483-492.
44. Hegner RE, Emlen ST, Demong NJ, (1982) Spatial organization of the white-fronted bee-eater. Nature, 298, 264-266.
45. Hohmann G, (1989) Group fission in Nilgiri langurs (Presbytis johnii). International Journal of Primatology, 10, 441-454.
46. Holekamp KE, Ogutu JO, Dublin HT, Frank LG, Smale L, (1993) Fission of a spotted hyena clan: consequences of prolonged female absenteeism and causes of female emigration. Ethology, 93, 285-299.
47. Hood GM, (2010) PopTools. Available from http://www.poptools.org.
48. Iwamoto T, Mori A, Kawai M, Bekele A, (1996) Anti-predator behavior of gelada baboons. Primates, 37, 389-397.
49. Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
50. Jombart T, (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
51. Jombart T, Ahmed I, (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics, 27, 3070-3071.
52. Jombart T, Devillard S, Balloux F, (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC genetics, 11, 94.
53. Kawai M, Dunbar RIM, Ohsawa H, Mori U, (1983) Social organization of gelada baboons: social units and definitions. Primates, 24, 13-24.
54. Kerth G, Perony N, Schweitzer F, (2011) Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proceedings of the Royal Society of London B: Biological Sciences, 278, 2761-2767.
55. Komdeur J, Edelaar P, (2001) Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment. Behavioral Ecology, 12, 706-715.
56. Koyama N, (1970) Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates, 11, 335-390.
57. Koyama N, (2003) Matrilineal cohesion and social networks in Macaca fuscata. International Journal of Primatology, 24, 797-811.
58. Krützen M, Sherwin W, Berggren P, Gales N, (2004) Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Marine Mammal Science, 20, 28-47.
59. Krützen M, Sherwin WB, Connor RC, et al,. (2003) Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proceedings of the Royal Society of London B: Biological Sciences, 270, 497-502.
60. Kummer H, (1984) From laboratory to desert and back: a social system of hamadryas baboons. Animal Behaviour, 32, 965-971.
61. Langergraber KA, (2012) Cooperation among kin. In: The Evolution of Primate Societies (eds, Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB,), pp. 491-513. University of Chicago Press, Chicago, Illinois.
62. Langergraber KE, Mitani JC, Vigilant L, (2007a) The limited impact of kinship on cooperation in wild chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 104, 7786.
63. Langergraber KE, Siedel H, Mitani JC, et al,. (2007b) The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS ONE, 2, e973.
64. Langergraber K, Mitani J, Vigilant L, (2009) Kinship and social bonds in female chimpanzees (Pan troglodytes). American Journal of Primatology, 71, 840-851.
65. Le Roux A, Beehner JC, Bergman TJ, (2011) Female philopatry and dominance patterns in wild geladas. American Journal of Primatology, 73, 422-430.
66. Lefebvre D, Ménard N, Pierre J, (2003) Modelling the influence of demographic parameters on group structure in social species with dispersal asymmetry and group fission. Behavioral Ecology and Sociobiology, 53, 402-410.
67. Li J, Wang Q, Han D, (1996) Fission in a free-ranging Tibetan macaque troop at Huangshan Mountain, China. Chinese Science Bulletin, 41, 1377-1381.
68. Lukas D, Reynolds V, Boesch C, Vigilant L, (2005) To what extent does living in a group mean living with kin? Molecular Ecology, 14, 2181-2196.
69. Mantel N, (1967) The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209-220.
70. Metheny JD, Kalcounis-Rueppell MC, Bondo KJ, Brigham RM, (2008) A genetic analysis of group movement in an isolated population of tree-roosting bats. Proceedings of the Royal Society of London B: Biological Sciences, 275, 2265-2272.
71. Möller LM, Beheregaray LB, (2004) Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Molecular Ecology, 13, 1607-1612.
72. Mori A, Iwamoto T, Bekele A, (1997) A case of infanticide in a recently found gelada population in Arsi, Ethiopia. Primates, 38, 79-88.
73. Nussey DH, Coltman DW, Coulson T, et al,. (2005) Rapidly declining fine-scale spatial genetic structure in female red deer. Molecular Ecology, 14, 3395-3405.
74. Ohsawa H, (1979) Herd dynamics. In: Contributions to Primatology: Ecological and Sociological Studies of Gelada Baboons (ed., Kawai M,), pp. 47-80. Karger, Basel.
75. Okamoto K, Matsumura S, (2001) Group fission in moor macaques (Macaca maurus). International Journal of Primatology, 22, 481-493.
76. Painter JN, Crozier RH, Poiani A, Robertson RJ, Clarke MF, (2000) Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Molecular Ecology, 9, 1339-1347.
77. Pappano DJ, Snyder-Mackler N, Bergman TJ, Beehner JC, (2012) Social "predators" within a multilevel primate society. Animal Behaviour, 84, 653-658.
78. Peakall R, Smouse P, (2012) GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 1, 6-8.
79. Pomeroy PP, Wilmer JW, Amos W, Twiss SD, (2001) Reproductive performance links to fine-scale spatial patterns of female grey seal relatedness. Proceedings of the Royal Society of London B: Biological Sciences, 268, 711-717.
80. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
81. Queller DC, Goodnight KF, (1989) Estimating relatedness using genetic markers. Evolution, 43, 258-275.
82. Quinn JL, Cresswell W, (2006) Testing domains of danger in the selfish herd: sparrowhawks target widely spaced redshanks in flocks. Proceedings of the Royal Society of London B: Biological Sciences, 273, 2521-2526.
83. Randall DA, Pollinger JP, Argaw K, Macdonald DW, Wayne RK, (2009) Fine-scale genetic structure in Ethiopian wolves imposed by sociality, migration, and population bottlenecks. Conservation Genetics, 11, 89-101.
84. Ratnayeke S, Tuskan GA, Pelton MR, (2002) Genetic relatedness and female spatial organization in a solitary carnivore, the raccoon, Procyon lotor. Molecular Ecology, 11, 1115-1124.
85. Roberts E, Lu A, Bergman T, Beehner J, (2012) A Bruce effect in wild geladas. Science, 335, 1222-1225.
86. Robinson J, (1988) Demography and group structure in wedgecapped capuchin monkeys, Cebus olivaceus. Behaviour, 104, 202-232.
87. Robinson SJ, Samuel MD, Lopez DL, Shelton P, (2012) The walk is never random: subtle landscape effects shape gene flow in a continuous white-tailed deer population in the Midwestern United States. Molecular Ecology, 21, 4190-4205.
88. Ron T, Henzi SP, Motro U, (1994) A new model of fission in primate troops. Animal Behaviour, 47, 223-226.
89. Rubenstein D, Hack M, (2004) Natural and sexual selection and the evolution of multi-level societies: insights from zebras with comparisons to primates. In: Sexual Selectin in Primates: New and Comparative Perspectives (eds, Kappeler PM, van Schaik CP,), pp. 266-279. Cambridge University Press, Cambridge, UK.
90. Schreier AL, Swedell L, (2009) The fourth level of social structure in a multi-level society: ecological and social functions of clans in hamadryas baboons. American Journal of Primatology, 71, 948-955.
91. Shotake T, Nozawa K, (1984) Blood protein variations in baboons. II. Genetic variability within and among herds of gelada baboons in the central Ethiopian plateau. Journal of Human Evolution, 13, 265-274.
92. Sigg H, Stolba A, Abegglen J-J, Dasser V, (1982) Life history of hamadryas baboons: Physical development, infant mortality, reproductive parameters and family relationships. Primates, 23, 473-487.
93. Silk JB, Alberts SC, Altmann J, (2003) Social bonds of female baboons enhance infant survival. Science, 302, 1231-1234.
94. Silk JB, Beehner JC, Bergman TJ, et al,. (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society of London B: Biological Sciences, 276, 3099-3104.
95. Silk JB, Beehner JC, Bergman TJ, et al,. (2010) Strong and consistent social bonds enhance the longevity of female baboons. Current Biology, 20, 1359-1361.
96. Snyder-Mackler N, Beehner J, Bergman T, (2012) Defining higher levels in the multilevel societies of geladas (Theropithecus gelada). International Journal of Primatology, 33, 1054-1068.
97. Sutherland DR, Spencer PBS, Singleton GR, Taylor AC, (2005) Kin interactions and changing social structure during a population outbreak of feral house mice. Molecular Ecology, 14, 2803-2814.
98. Swedell L, Saunders J, Schreier A, et al,. (2011) Female "dispersal" in hamadryas baboons: transfer among social units in a multilevel society. American Journal of Physical Anthropology, 145, 360-370.
99. Tinsley Johnson E, Snyder-Mackler N, Beehner JC, Bergman TJ, (2014) Kinship and dominance rank influence the strength of social bonds in female geladas. International Journal of Primatology, 35, 288-304.
100. Van De Casteele T, Galbusera P, Matthysen E, (2001) A comparison of microsatellite-based pairwise relatedness estimators. Molecular Ecology, 10, 1539-1549.
101. Van Horn R, Buchan J, Altmann J, Alberts S, (2007) Divided destinies: Group choice by female savannah baboons during social group fission. Behavioral Ecology and Sociobiology, 61, 1823-1837.
102. Wang J, (2002) An estimator for pairwise relatedness using molecular markers. Genetics, 160, 1203-1215.
103. Wang J, (2011) coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources, 11, 141-145.
104. West Eberhard MJ, (1975) The evolution of social behavior by kin selection. The Quarterly Review of Biology, 50, 1-33.
105. Whitehead H, Antunes R, Gero S, et al,. (2012) Multilevel societies of female sperm whales (Physeter macrocephalus) in the Atlantic and Pacific: why are they so different? International Journal of Primatology, 33, 1142-1164.
106. Widdig A, Nürnberg P, Bercovitch F, et al,. (2006) Consequences of group fission for the patterns of relatedness among rhesus macaques. Molecular Ecology, 15, 3825-3832.
107. Wittemyer G, Douglas-Hamilton I, Getz WM, (2005) The socioecology of elephants: analysis of the processes creating multitiered social structures. Animal Behaviour, 69, 1357-1371.
108. Wittemyer G, Okello J, Rasmussen HB, et al,. (2009) Where sociality and relatedness diverge: the genetic basis for hierarchical social organization in African elephants. Proceedings of the Royal Society of London B: Biological Sciences, 276, 3513-3521.