Male-Mediated gene flow in patrilocal primates

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Schubert, Grit ^a,b   Stoneking, Colin J ^c   Arandjelovic, Mimi ^a   Boesch, Christophe ^a   Eckhardt, Nadin ^a   Hohmann, Gottfried ^a   Langergraber, Kevin ^a,d   Lukas, Dieter ^e   Vigilant, Linda ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c EMMANUEL COLLEGE   (United Kingdom)

^d Boston University   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; FEMALE; GENE FLOW; GENE MUTATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; MALE; NONHUMAN; PAN PANISCUS; PATERNITY; PRIMATE; REPRODUCTION; SEX DIFFERENCE; SIMULATION; SPECIES DIFFERENCE; Y CHROMOSOME; ANIMAL; GENETICS; PAN TROGLODYTES; SEXUAL DEVELOPMENT;

PAN; PAN PANISCUS; PAN TROGLODYTES VERUS; PRIMATES;

MICROSATELLITE DNA;

ANIMALS; FEMALE; GENE FLOW; GENETIC VARIATION; HAPLOTYPES; MALE; MICROSATELLITE REPEATS; PAN PANISCUS; PAN TROGLODYTES; SEX CHARACTERISTICS; Y CHROMOSOME;

EID: 79959799617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021514     Document Type: Article

References (99)

1. Pusey AE, Wolf M, (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution 11: 201-206.
2. Lawson Handley LJL, Perrin N, (2007) Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology 16: 1559-1578.
3. Clobert J, Danchin E, Dhondt AA, Nichols JD, (2001) Dispersal. Oxford Oxford University Press.
4. Hamilton WD, (1964) The genetical evolution of social behaviour II. Journal of Theoretical Biology 7: 17-52.
5. Greenwood PJ, (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28: 1140-1162.
6. Silk JB, Alberts SC, Altmann J, (2003) Social bonds of female baboons enhance infant survival. Science 302: 1231-1234.
7. McCracken GF, Bradbury JW, (1981) Social organization and kinship in the polygynous bat Phyllostomus hastatus. Behavioral Ecology and Sociobiology 8: 11-34.
8. Favre L, Balloux Fo, Goudet J, Perrin N, (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proceedings of the Royal Society B: Biological Sciences 264: 127-132.
9. Strier KB, (1990) New World primates, new frontiers: Insights from the woolly spider monkey, or muriqui (Brachyteles arachnoides). International Journal of Primatology 11: 7-19.
10. Symington MM, (1987) Sex ratio and maternal rank in wild spider monkeys: When daughters disperse. Behavioral Ecology and Sociobiology 20: 421-425.
11. Fedigan L, Baxter M, (1984) Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25: 279-294.
12. Nishimura A, (2003) Reproductive parameters of wild female Lagothrix lagotricha. International Journal of Primatology 24: 707-722.
13. Hammond RL, Lawson Handley LJ, Winney BJ, Bruford MW, Perrin N, (2006) Genetic evidence for female-biased dispersal and gene flow in a polygynous primate. Proceedings of the Royal Society B: Biological Sciences 273: 479-484.
14. Struhsaker TT, (1975) The Red Colobus Monkey. Chicago University of Chicago Press.
15. Kano T, (1982) The social group of pygmy chimpanzees (Pan paniscus). Primates 23: 171-188.
16. Pusey AE, (1979) Intercommunity transfer of chimpanzees in Gombe National Park. In: Hamburg D, McCown E, editors. The Great Apes Menlo Park Benjamin/Cummings pp. 465-479.
17. Murdock GP, (1981) Atlas of World Cultures University of Pittsburgh Press.
18. Rodseth L, Wrangham RW, Harrigan AM, Smuts BB, (1991) The human community as a primate society. Current Anthropology 32: 221-254.
19. Foley RA, (1989) The evolution of hominid social behaviour. In: Standen V, Foley RA, editors. Comparative Socioecology Oxford Blackwell Scientific Publications pp. 473-494.
20. Di Fiore A, (2003) Molecular genetic approaches to the study of primate behavior, social organization, and reproduction. American Journal of Physical Anthropology 122: 62-99.
21. DeYoung RW, Honeycutt RL, (2005) The molecular toolbox: Genetic techniques in wildlife ecology and management. Journal of Wildlife Management 69: 1362-1384.
22. Gauffre B, Petit E, Brodier S, Bretagnolle V, Cosson JF, (2009) Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proceedings of the Royal Society B: Biological Sciences 276: 3487-3494.
23. Coulon A, Cosson JF, Morellet N, Angibault JM, Cargnelutti B, et al. (2006) Dispersal is not female biased in a resource-defence mating ungulate, the European roe deer. Proceedings of the Royal Society B: Biological Sciences 273: 341-348.
24. Guschanski K, Caillaud D, Robbins MM, Vigilant L, (2008) Females shape the genetic structure of a gorilla population. Current Biology 18: 1809-1814.
25. Di Fiore A, Link A, Schmitt CA, Spehar SN, (2009) Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data. Behaviour 146: 437-470.
26. Wimmer B, Tautz D, Kappeler P, (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behavioral Ecology and Sociobiology 52: 166-175.
27. Melnick DJ, Hoelzer GA, Absher R, Ashley MV, (1993) MtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Molecular Biology and Evolution 10: 282-295.
28. Wilkins JF, Marlowe FW, (2006) Sex-biased migration in humans: what should we expect from genetic data? BioEssays 28: 290-300.
29. Ségurel L, Martínez-Cruz B, Quintana-Murci L, Balaresque P, Georges M, et al. (2008) Sex-specific genetic structure and social organization in central Asia: Insights from a multi-locus study. PLoS Genetics 4: e1000200.
30. Jack KM, Fedigan LM, (2009) Female dispersal in a female-philopatric species, Cebus capucinus. Behaviour 146: 471-497.
31. Nagy M, Heckel G, Voigt CC, Mayer F, (2007) Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny. Proceedings of the Royal Society of London Series B: Biological Sciences 274: 3019-3025.
32. Holekamp KE, (1984) Natal dispersal in Belding's ground squirrels (Spermophilus beldingi). Behavioral Ecology and Sociobiology 16: 21-30.
33. Harris TR, Caillaud D, Chapman CA, Vigilant L, (2009) Neither genetic nor observational data alone are sufficient for understanding sex-biased dispersal in a social-group-living species. Molecular Ecology 18: 1777-1790.
34. Van Horn RC, 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.
35. Isvaran K, Clutton-Brock T, (2007) Ecological correlates of extra-group paternity in mammals. Proceedings of the Royal Society B: Biological Sciences 274: 219-224.
36. Ostner J, Nunn CL, Schulke O, (2008) Female reproductive synchrony predicts skewed paternity across primates. Behavioral Ecology 19: 1150-1158.
37. Goodall J, Bandora A, Bergman E, Busse C, Matama H, et al. (1979) Intercommunity interactions in the chimpanzee population of the Gombe National Park. In: Hamburg D, McCown ER, editors. The Great Apes Menlo Park Benjamin/Cummings pp. 13-53.
38. Newton-Fisher NE, (1999) Infant killers of Budongo. Folia Primatologica 70: 167-169.
39. Watts DP, Mitani JC, (2001) Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138: 299-327.
40. Muller MN, (2002) Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant L, editors. Behavioural Diversity in Chimpanzees and Bonobos Cambridge Cambridge University Press pp. 112-124.
41. Boesch C, Crockford C, Herbinger I, Wittig R, Moebius Y, et al. (2008) Intergroup conflicts among chimpanzees in Taï National Park: lethal violence and the female perspective. American Journal of Primatology 70: 519-532.
42. Idani G, (1990) Relations between unit-groups of bonobos at Wamba, Zaire: Encounters and temporary fusions. African Study Monographs 11: 153-186.
43. Kano T, (1992) The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Princeton, NJ Princeton University Press.
44. Hohmann G, (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42: 91-99.
45. Hohmann G, Fruth B, (2002) Dynamics of social organization in bonobos (Pan paniscus). In: Boesch C, Hohmann G, Marchant LF, editors. Behavioural Diversity in Chimpanzees and Bonobos Cambridge Cambridge University Press pp. 138-149.
46. Nishida T, Hiraiwa-Hasegawa M, Hasegawa T, Takahata Y, (1985) Group extinction and female transfer in wild chimpanzees in the Mahale Mountains National Park, Tanzania. Zeitschrift für Tierpsychologie 67: 281-301.
47. Emery-Thompson M, Newton-Fisher N, Reynolds V, (2006) Probable community transfer of parous adult female chimpanzees in the Budongo Forest, Uganda. International Journal of Primatology 27: 1601-1617.
48. Boesch C, (2009) The Real Chimpanzee: Sex Strategies in the Forest. Cambridge Cambridge University Press.
49. Wilson ML, Wrangham RW, (2003) Intergroup relations in chimpanzees. Annual Review of Anthropology 32: 363-392.
50. Townsend SW, Slocombe KE, Emery Thompson M, Zuberbühler K, (2007) Female-led infanticide in wild chimpanzees. Current Biology 17: R355-R356.
51. Goodall J, (1986) The Chimpanzees of Gombe. Cambridge Harvard University Press.
52. Nishida T, Takasaki H, Takahata Y, (1990) Chimpanzees of the Mahale Mountains; Nishida T, ed. Tokyo University Press of Tokyo.
53. Boesch C, Boesch-Achermann H, (2000) The Chimpanzees of the Taï Forest: Behavioural Ecology and Evolution. Oxford Oxford University Press.
54. Boesch C, Kohou G, Néné H, Vigilant L, (2006) Male competition and paternity in wild chimpanzees of the Taï Forest. American Journal of Physical Anthropology 130: 103-115.
55. 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.
56. Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D, (1999) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proceedings of the Royal Society B: Biological Sciences 266: 1189-1195.
57. Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, et al. (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour 77: 873-885.
58. Newton-Fisher NE, Emery Thompson M, Reynolds V, Boesch C, Vigilant L, (2010) Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. American Journal of Physical Anthropology 142: 417-428.
59. Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, et al. (1994) Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265: 1193-1201.
60. Eriksson J, Hohmann G, Boesch C, Vigilant L, (2004) Rivers influence the population genetic structure of bonobos (Pan paniscus). Molecular Ecology 13: 3425-3435.
61. Eriksson J, Siedel H, Lukas D, Kayser M, Erler A, 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.
62. Langergraber KE, Siedel H, Mitani JC, Wrangham RW, Reynolds V, et al. (2007) The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS One 2: 1-10.
63. 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.
64. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, et al. (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology 13: 2089-2094.
65. Hohmann G, Fruth B, (2003) LuiKotal - a new site for field research on bonobos in the Salonga National Park. Pan African News 10: 25-27.
66. Morin PA, Chambers KE, Boesch C, Vigilant L, (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Molecular Ecology 10: 1835-1844.
67. Packer C, Hilborn R, Mosser A, Kissui B, Borner M, et al. (2005) Ecological change, group territoriality, and population dynamics in Serengeti lions. Science 307: 390-393.
68. Bradley BJ, Chambers KE, Vigilant L, (2001) Accurate DNA-based sex identification of apes using non-invasive samples. Conservation Genetics 2: 179-181.
69. Arandjelovic M, Guschanski K, Schubert G, Harris TR, Thalmann O, et al. (2009) Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Molecular Ecology Resources 9: 28-36.
70. Arandjelovic M, Head J, Rabanal LI, Schubert G, Mettke E, et al. (2011) Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE 6: e14761.
71. Kalinowski ST, Taper ML, Marshall TC, (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16: 1099-1106.
72. Excoffier L, Laval G, Schneider S, (2005) ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
73. Wright S, (1943) Isolation by distance. Genetics 28: 114-138.
74. Hedrick PW, (2005) A standardized genetic differentiation measure. Evolution 59: 1633-1638.
75. Meirmans PG, (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60: 2399-2402.
76. Wilson IJ, Weale ME, Balding DJ, (2003) Inferences from DNA data: population histories, evolutionary processes and forensic match probabilities. Journal of the Royal Statistical Society A: Statistics in Society 166: 155-188.
77. Kayser M, Vowles EJ, Kappei D, Amos W, (2006) Microsatellite length differences between humans and chimpanzees at autosomal loci are not found at aquivalent haploid Y chromosomal loci. Genetics 173: 2179-2186.
78. Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, et al. (1996) Behavior predicts genes structure in a wild primate group. Proceedings of the National Academy of Sciences of the United States of America 93: 5797-5801.
79. Hill K, Hurtado AM, (1996) Ache Life History: The Ecology and Demography of a Foraging People. Hawthorne, NY Aldine de Gruyter.
80. Clutton-Brock TH, (1988) Reproductive Success; Clutton-Brock TH, ed. Chicago University of Chicago Press.
81. Douadi MI, Gatti S, Levrero F, Duhamel G, Bermejo M, et al. (2007) Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla). Molecular Ecology 16: 2247-2259.
82. Radespiel U, Rakotondravony R, Chikhi L, (2008) Natural and anthropogenic determinants of genetic structure in the largest remaining population of the endangered golden-brown mouse lemur, Microcebus ravelobensis. American Journal of Primatology 70: 860-870.
83. Pilot M, Jedrzejewski W, Branicki W, Sidorovich VE, Jedrzejewska B, et al. (2006) Ecological factors influence population genetic structure of European grey wolves. Molecular Ecology 15: 4533-4553.
84. Hey J, (2010) The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Molecular Biology and Evolution 27: 921-933.
85. Wegmann D, Excoffier L, (2010) Bayesian inference of the demographic history of chimpanzees. Molecular Biology and Evolution 27: 1425-1435.
86. Cant MA, Otali E, Mwanguhya F, (2001) Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo). Journal of Zoology 254: 155-162.
87. Möller LM, Beheregaray LB, (2004) Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Molecular Ecology 13: 1607-1612.
88. Sweitzer RA, Berger J, (1998) Evidence for female-biased dispersal in North American porcupines (Erethizon dorsatum). Journal of Zoology 244: 159-166.
89. Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR, (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society B: Biological Sciences 272: 1217-1226.
90. Goossens B, Graziani L, Waits LP, Farand E, Magnolon S, et al. (1998) Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behavioral Ecology and Sociobiology 43: 281-288.
91. Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, et al. (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behavioral Ecology and Sociobiology 49: 8-17.
92. Munshi-South J, (2007) Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew. Behavioral Ecology and Sociobiology 62: 201-212.
93. Young AJ, Spong G, Clutton-Brock T, (2007) Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal. Proceedings of the Royal Society B: Biological Sciences 274: 1603-1609.
94. Soulsbury CD, (2010) Genetic patterns of paternity and testes size in mammals. PLoS One 5: 1-6.
95. Clutton-Brock TH, Isvaran K, (2006) Paternity loss in contrasting mammalian societies. Biology Letters 2: 513-516.
96. Marlowe FW, (2004) Marital residence among foragers. Current Anthropology 45: 277-284.
97. Hohmann G, Fruth B, (2003) Culture in bonobos? Between-species and within-species variation in behavior. Current Anthropology 44: 563-571.
98. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, et al. (1999) Cultures in chimpanzees. Nature 399: 682-685.
99. Langergraber KE, Boesch C, Inoue E, Inoue-Murayama M, Mitani JC, et al. (2010) Genetic and 'cultural' similarity in wild chimpanzees. Proceedings of the Royal Society B: Biological Sciences.