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The Effects of Dispersal and Reproductive Patterns on the Evolution of Male Sociality in White-Faced Capuchins

  • Eva C. WikbergEmail author
  • Katharine M. Jack
  • Linda M. Fedigan
  • Shoji Kawamura
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

In many mammalian species, philopatric females reside with female kin with whom they form long-lasting cooperative bonds, whereas dispersing males rarely form strong bonds with other males. However, males may have the opportunity to disperse and form long-lasting bonds with paternal male kin in species with high male reproductive skew and parallel male dispersal. We used 54 group-years with demographic and genetic data to investigate how male dispersal and reproductive patterns affected the distribution of male kin in the Santa Rosa white-faced capuchins (Cebus capucinus imitator). During 41 of 54 group-years, there was a high degree of reproductive monopolization by either the alpha or a subordinate male. Natal males often co-resided with paternal brothers of similar age. The likelihood of parallel dispersal from the natal group increased with age similarity and paternal sibship. Some males may possibly gain inclusive fitness benefits by engaging in parallel dispersal and forming long-term cooperative bonds with other males. However, only one of three groups displayed a positive association between male-male relatedness and time spent co-resident in the breeding group. Inbreeding avoidance between alpha males and their daughters also gives subordinate males an opportunity to gain direct fitness benefits and may provide a strong incentive for cooperation among males that are not close kin. These findings suggest that cooperation between related and unrelated males likely evolved due to different reasons. Subordinate males related to the alpha male may gain inclusive fitness benefits, while only unrelated subordinate males gained reproductive opportunities and direct fitness benefits from cooperating.

Keywords

Social evolution Kin cooperation Kin competition Inbreeding Parallel dispersal 

Notes

Acknowledgements

This study was approved and supported by the University of Calgary’s Life and Environmental Sciences Animal Care Committee, Tulane University’s Institutional Animal Care and Use Committee, the Costa Rican Park Service, and Roger Blanco Segura and the administration of the Área de Conservación Guanacaste. The lab work was funded by the Japan Society for Promotion of Science’s Postdoctoral Fellowship (ECW) and Grant-in-Aid (SK). The field work was funded by an NSERC Discovery Grant and the Canada Research Chairs Program (LMF) and by the LSB Leakey Foundation, Tulane University’s Department of Anthropology, Stone Center for Latin American Studies, Newcomb Institute, and Research Enhancement Fund (KMJ). We would like to thank the many students and research assistants who collected data in the field; Mackenzie Bergstrom, Fernando Campos, Tomohide Hiwatashi, and Akiko Yashima for the help with the lab work and Urs Kalbitzer and two anonymous reviewers for comments that improved earlier versions of this manuscript.

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723. https://doi.org/10.1109/TAC.1974.1100705 CrossRefGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefGoogle Scholar
  3. Barton K (2013) MuMIn: Multi-model inference. R package version 1.9.5. http://CRAN.R-project.org/package=MuMIn. Accessed 1 May 2017
  4. Bates D, Maechler M, Bolker B, Walker S, Bojesen Christensen RH, Singman H (2014) lme4: linear mixed-effects models using Eigen and S4. http://lme4.r-forge.r-project.org/. Accessed 1 June 2014
  5. Borgatti S, Everett M, Freeman L (2002) Ucinet for windows: software for social network analysis. Analytic Technologies, HarvardGoogle Scholar
  6. Brasington LF, Wikberg EC, Kawamura S, Fedigan LM, Jack KM (2017) Infant mortality in white-faced capuchins: the impact of alpha male replacements. Am J Primatol 79:e22725. https://doi.org/10.1002/ajp.22725 CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  8. Chapais B (2001) Primate nepotism: what is the explanatory value of kin selection? Int J Primatol 22:203–229. https://doi.org/10.1023/A:1005619430744 CrossRefGoogle Scholar
  9. Diaz-Munoz SL, Ribeiro AM (2014) No sex-biased dispersal in a primate with an uncommon social system-cooperative polyandry. PeerJ 2:UNSP e640. https://doi.org/10.7717/peerj.640 CrossRefGoogle Scholar
  10. Fedigan LM (1993) Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus). Int J Primatol 14:853–877. https://doi.org/10.1007/BF02220256 CrossRefGoogle Scholar
  11. Fedigan LM, Jack KM (2004) The demographic and reproductive context of male replacements in Cebus capucinus. Behaviour 141:755–775. https://doi.org/10.1163/1568539042245178 CrossRefGoogle Scholar
  12. Fedigan LM, Jack KM (2011) Two girls for every boy: the effects of group size and composition on the reproductive success of male and female white-faced capuchins. Am J Phys Anthropol 144:317–326. https://doi.org/10.1002/ajpa.21414 CrossRefPubMedGoogle Scholar
  13. Fedigan LM, Jack KM (2012) Tracking neotropical monkeys in Santa Rosa: lessons from a regenerating Costa Rican dry forest. In: Kappeler PM, Watts D (eds) Long-term field studies of primates. Springer, Dordrecht, pp 165–184CrossRefGoogle Scholar
  14. Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B (2012) Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Mol Ecol 21:3237–3249. https://doi.org/10.1111/j.1365-294X.2012.05593.x CrossRefPubMedGoogle Scholar
  15. Godoy I, Vigilant L, Perry S (2016) Inbreeding risk, avoidance and costs in a group-living primate, Cebus capucinus. Behav Ecol Sociobiol 70:1601–1611. https://doi.org/10.1007/s00265-016-2168-1 CrossRefGoogle Scholar
  16. Greenwood P (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. https://doi.org/10.1016/S0003-3472(80)80103-5 CrossRefGoogle Scholar
  17. Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21. https://doi.org/10.1016/S0169-5347(01)02355-2 CrossRefGoogle Scholar
  18. Gros-Louis J, Perry SE, Manson JH (2003) Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (Cebus capucinus). Primates 44:341–346. https://doi.org/10.1007/s10329-003-0050-z CrossRefPubMedGoogle Scholar
  19. Hamilton WD (1964a) The genetical evolution of social behaviour. J Theor Biol 7:1–52. https://doi.org/10.1016/0022-5193(64)90038-4 CrossRefPubMedGoogle Scholar
  20. Hamilton WD (1964b) The genetical evolution of social behaviour. II. J Theor Biol 7:17–52CrossRefGoogle Scholar
  21. Hanneman RA, Riddle M (2005) Introduction to social network methods. University of California, RiversideGoogle Scholar
  22. Hothorn T, Bretz F, Westfall P, Heiberger RM, Scheutzenmeister A (2014) Simultaneous Inference in General Parametric Models. http://lme4.r-forge.r-project.org/. Accessed 1 May 2017
  23. Jack KM (2003) Explaining variation in affiliative relationships among male white-faced capuchins (Cebus capucinus). Folia Primatol 74:1–16. https://doi.org/10.1159/000068390 CrossRefPubMedGoogle Scholar
  24. Jack KM, Fedigan LM (2004a) Male dispersal patterns in white-faced capuchins, Cebus capucinus part 2: patterns and causes of secondary dispersal. Anim Behav 67:771–782. https://doi.org/10.1016/j.anbehav.2003.06.015 CrossRefGoogle Scholar
  25. Jack KM, Fedigan LM (2004b) Male dispersal patterns in white-faced capuchins, Cebus capucinus part 1: patterns and causes of natal emigration. Anim Behav 67:761–769. https://doi.org/10.1016/j.anbehav.2003.04.015 CrossRefGoogle Scholar
  26. Jack KM, Fedigan LM (2006) Why be alpha male? Dominance and reproductive success in wild white-faced capuchins (Cebus capucinus). In: Estrada A, Garber P, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 367–386CrossRefGoogle Scholar
  27. Jack KM, Fedigan LM (2009) Female dispersal in a female-philopatric species, Cebus capucinus. Behaviour 146:471–497. https://doi.org/10.1163/156853909X404420 CrossRefGoogle Scholar
  28. Jack KM, Fedigan LM (2018, this volume) Alpha male capuchins (Cebus capucinus imitator) as keystone individuals. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 91–109Google Scholar
  29. Jack KM, Sheller C, Fedigan LM (2012) Social factors influencing natal dispersal in male white-faced capuchins (Cebus capucinus). Am J Primatol 74:359–365. https://doi.org/10.1002/ajp.20974 CrossRefPubMedGoogle Scholar
  30. Jack KM, Schoof VAM, Sheller CR, Rich CI, Klingelhofer PP, Ziegler TE, Fedigan L (2014) Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus). Gen Comp Endocrinol 195:58–67. https://doi.org/10.1016/j.ygcen.2013.10.010 CrossRefPubMedGoogle Scholar
  31. Kalbitzer U, Bergstrom ML, Carnegie SD, Wikberg EC, Kawamura S, Campos FA, Jack KM, Fedigan LM (2017) Female sociality and sexual conflict shape offspring survival in a Neotropical primate. Proc Natl Acad Sci U S A 114:1892–1897. https://doi.org/10.1073/pnas.1608625114 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kalinowski ST, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579. https://doi.org/10.1111/j.1471-8286.2006.01256.x CrossRefGoogle Scholar
  33. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x CrossRefPubMedGoogle Scholar
  34. Kulik L, Amici F, Langos D, Widdig A (2015) Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta). Int J Primatol 36:353–376. https://doi.org/10.1007/s10764-015-9826-4 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655. https://doi.org/10.1046/j.1365-294x.1998.00374.x CrossRefPubMedGoogle Scholar
  36. Meikle DB, Vessey SH (1981) Nepotism among rhesus monkey brothers. Nature 294:160–161. https://doi.org/10.1038/294160a0 CrossRefPubMedGoogle Scholar
  37. 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:R156–R157. https://doi.org/10.1016/j.cub.2006.02.055 CrossRefPubMedGoogle Scholar
  38. Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, Vigilant L (2010) Male dominance and reproductive success in wild white-faced capuchins (Cebus capucinus) at Lomas Barbudal, Costa Rica. Am J Primatol 72:1118–1130. https://doi.org/10.1002/ajp.20876 CrossRefPubMedGoogle Scholar
  39. Murray CM, Lonsdorf EV, Stanton MA, Wellens KR, Miller JA, Goodall J, Pusey AE (2016) Early social exposure in wild chimpanzees: mothers with sons are more gregarious than mothers with daughters. Proc Natl Acad Sci U S A 111:18189–18194CrossRefGoogle Scholar
  40. Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. Am Nat 156:577–589. https://doi.org/10.1086/316995 CrossRefPubMedGoogle Scholar
  41. Perry S (1998) Male-male social relationships in wild white-faced capuchins, Cebus capucinus. Behaviour 135:139–172CrossRefGoogle Scholar
  42. Perry S (2012) The behavior of wild white-faced capuchins: demography, life history, social relationships, and communication. In: Brockmann HJ, Naguib M, Mitani JC, Simmons LW (eds) Advances in the study of behavior. Academic, Burlington, pp 135–181Google Scholar
  43. Robinson SP, Simmons LW, Kennington WJ (2013) Estimating relatedness and inbreeding using molecular markers and pedigrees: the effect of demographic history. Mol Ecol 22:5779–5792. https://doi.org/10.1111/mec.12529 CrossRefPubMedGoogle Scholar
  44. Schoof VAM, Jack KM (2014) Male social bonds: strength and quality among co-resident white-faced capuchin monkeys (Cebus capucinus). Behaviour 151:963–992. https://doi.org/10.1163/1568539X-00003179 CrossRefGoogle Scholar
  45. Schoof VAM, Wikberg EC, Fedigan LM, Jack KM, Ziegler TE, Kawamura S (2015) Infanticides during periods of social stability: kinship, resumption of ovarian cycling, and mating access in white-faced capuchins (Cebus capucinus). Neotropical Primates 21:192–196Google Scholar
  46. Schuelke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210. https://doi.org/10.1016/j.cub.2010.10.058 CrossRefGoogle Scholar
  47. Sharp SP, Simeoni M, Hatchwell BJ (2008) Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird. Proc R Soc B Biol Sci 275:2125–2130. https://doi.org/10.1098/rspb.2008.0398 CrossRefGoogle Scholar
  48. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234. https://doi.org/10.1126/science.1088580 CrossRefPubMedGoogle Scholar
  49. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc B-Biol Sci 276:3099–3104. https://doi.org/10.1098/rspb.2009.0681 CrossRefGoogle Scholar
  50. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309. https://doi.org/10.1007/s002650050390 CrossRefGoogle Scholar
  51. Teichroeb JA, Wikberg EC, Sicotte P, Ting N (2014) Factors influencing male affiliation and coalitions in a species with male dispersal and intense male-male competition, Colobus vellerosus. Behaviour 151:1045–1066. https://doi.org/10.1163/1568539X-00003089 CrossRefGoogle Scholar
  52. van Noordwijk MA, van Schaik CP (2001) Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138:359–395. https://doi.org/10.1163/15685390152032505 CrossRefGoogle Scholar
  53. van Schaik CP (1989) Social evolution in primates: the role of ecological factors and male behaviour. Proc Br Acad 88:9–31Google Scholar
  54. West SA, Pen I, Griffin AS (2002) Conflict and cooperation - cooperation and competition between relatives. Science 296:72–75. https://doi.org/10.1126/science.1065507 CrossRefPubMedGoogle Scholar
  55. Widdig A (2013) The impact of male reproductive skew on kin structure and sociality in multi-male groups. Evol Anthropol 22:239–250CrossRefGoogle Scholar
  56. Widdig A, Langos D, Kulik L (2016) Sex differences in kin bias at maturation: male rhesus macaques prefer paternal kin prior to natal dispersal. Int J Primatol 78:78–91CrossRefGoogle Scholar
  57. Wikberg EC, Sicotte P, Campos FA, Ting N (2012) Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white Colobus monkey (Colobus vellerosus). PLoS One 7:e48740. https://doi.org/10.1371/journal.pone.0048740 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Wikberg EC, Jack KM, Campos FA, Fedigan LM, Sato A, Bergstrom ML, Hiwatashi T, Kawamura S (2014a) The effect of male parallel dispersal on the kin composition of groups in white-faced capuchins. Anim Behav 96:9–17. https://doi.org/10.1016/j.anbehav.2014.07.016 CrossRefGoogle Scholar
  59. Wikberg EC, Ting N, Sicotte P (2014b) Familiarity is more important than phenotypic similarity in shaping social relationships in a facultative female dispersed primate, Colobus vellerosus. Behav Process 106:27–35. https://doi.org/10.1016/j.beproc.2014.04.002 CrossRefGoogle Scholar
  60. Wikberg EC, Jack KM, Fedigan LM, Campos FA, Yashima AS, Bergstrom ML, Hiwatashi T, Kawamura S (2017) Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator). Mol Ecol 26:653–667. https://doi.org/10.1111/mec.13898 CrossRefPubMedGoogle Scholar
  61. Wrangham R (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300. https://doi.org/10.1163/156853980X00447 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Eva C. Wikberg
    • 1
    Email author
  • Katharine M. Jack
    • 2
  • Linda M. Fedigan
    • 3
  • Shoji Kawamura
    • 4
  1. 1.Department of AnthropologyUniversity of Texas at San AntonioSan AntonioUSA
  2. 2.Department of AnthropologyTulane UniversityNew OrleansUSA
  3. 3.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  4. 4.Department of Integrated BiosciencesUniversity of TokyoKashiwaJapan

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