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Fathers enhance social bonds among paternal half-siblings in immature olive baboons (Papio hamadryas anubis)

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Abstract

A universal aspect of mammalian sociality is substantive, core relationships among relatives. Although comparative studies of nonhuman primates have clarified the adaptive importance of kinship, previous research has focused primarily on maternal relatives. To rectify this gap in the literature, recent work has begun to examine the social and adaptive consequences of paternal kinship. However, among multimale-multifemale species, particularly Old World primates, there have been conflicting reports describing the social bonds among paternal relatives. Some researchers have suggested that this inconsistency results from the availability of preferred relatives (maternal kin) as social partners. To explore this hypothesis, we examine the relationship between the availability of kin and sociality among immature olive baboons (Papio hamadryas anubis) by considering the effects that parents have on the social bonds among young maternal and paternal half-siblings. We found that while the presence of a mother in the group did not affect social bonds among immatures, the presence of a father did have a significant impact. Compared to immatures whose fathers were absent from the group, individuals with a father present maintained stronger bonds with paternal half-siblings. These data may help explain some of the variation in previous results among different studies examining the social bonds of half-siblings. Furthermore, our study suggests that the development of relationships among paternal half-siblings is facilitated by fathers and that relationships with paternal kin may be just as critical as those with maternal kin.

Significance statement

This study indicates that even in a social system in which matrilineal kinship powerfully influences group structure and dynamics, paternal kinship may nevertheless form the basis of significant selective forces in social evolution.

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Reference

  • Alberts SC (1999) Paternal kin discrimination in wild baboons. Proc R Soc Lond B 266:1501–1506

    Article  CAS  Google Scholar 

  • Alberts SC, Watts H, Altmann J (2003) Queuing and queue jumping: long term patterns of reproductive skew among male savannah baboons. Anim Behav 65:821–840

    Article  Google Scholar 

  • Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265

    Article  CAS  PubMed  Google Scholar 

  • Altmann J (1979) Age cohorts as paternal sibships. Behav Ecol Sociobiol 6:161–169

    Article  Google Scholar 

  • Archie EA, Tung J, Clark M, Altmann J, Alberts SC (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc B 281:20141261

    Article  PubMed  PubMed Central  Google Scholar 

  • Aureli F, Fraser ON, Schaffner C, Schino G (2012) The regulation of social relationships. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 531–551

    Google Scholar 

  • Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1(7), http://cran.r-project.org/web/packages/lme4/lme4.pdf

  • Borries C, Laundhardt K, Epplen JT, Winkler P (1999) Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups-defense pattern, paternity and sexual behaviour. Behav Ecol Sociobiol 46:350–356

    Article  Google Scholar 

  • Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multimale primate society. Nature 425:179–181

    Article  CAS  PubMed  Google Scholar 

  • Chapais B, Berman CM (2004) Kinship and behavior in primates. Oxford University Press, New York

    Google Scholar 

  • Charpentier MJE, Peignot P, Hossaert-McKey M, Wickings EJ (2007) Kin discrimination in immature mandrills, Mandrillus sphinx. Anim Behav 73:37–45

    Article  Google Scholar 

  • Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008) Paternal effects on offspring fitness in a multimale primate society. P Natl Acad Sci USA 105:1988–1992

    Article  CAS  Google Scholar 

  • Charpentier MJE, Huchard E, Widdig A, Gimenez O, Sallé B, Kappeler P, Renoult JP (2012) Distribution of affiliative behavior across kin classes and their fitness consequences in mandrills. Ethology 118:1198–1207

    Article  Google Scholar 

  • Cheney DL (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behav Ecol Sociobiol 2:202–318

    Article  Google Scholar 

  • Cords M (2002) Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour 139:291–314

    Article  Google Scholar 

  • Dobson AJ (2002) An introduction to generalized linear models. Chapman and Hall, New York

  • Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL (2006) Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc R Soc Lond B 273:707–712

    Article  CAS  Google Scholar 

  • Fickenscher G, Ferreira da Silva M, Patzelt A, Roos C, Fischer J, Zinner D (2011) Genetic evidence for male philopatry in Guinea baboons. Folia Primatol 82:365

    Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. SAGE, Thousand Oaks

    Google Scholar 

  • Gouzoules S, Gouzoules H (1987) Kinship. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 299–305

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior, I and II. J Theor Biol 7:1–52

    Article  CAS  PubMed  Google Scholar 

  • Henzi SP, Lycett JE, Weingrill T (1997a) Cohort size and the allocation of social effort by female mountain baboons. Anim Behav 54:1235–1243

    Article  CAS  PubMed  Google Scholar 

  • Henzi SP, Lycett JE, Piper SE (1997b) Fission and troop size in a mountain baboon population. Anim Behav 53:525–535

    Article  Google Scholar 

  • Hill DA (2004) The effects of demographic variation on kinship structure and behavior in cercopithecines. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, New York, pp 132–150

    Google Scholar 

  • Holmes WG, Sherman PW (1983) Kin recognition in animals. Am Sci 71:46–55

    Google Scholar 

  • Huchard E, Charpentier MJ, Marshall H, King AJ, Knapp LA, Cowlishaw G (2013) Paternal effects on access to resources in a promiscuous primate society. Behav Ecol 24:229–236

    Article  Google Scholar 

  • Iddi S, Doku-Amponsah K (2015) Statistical model for overdispersed count outcome with many zeros: an approach for direct marginal inference. arXiv:1504.00071

  • Kopp GH, Ferreira da Silva MJ, Fischer J, Brito JC, Regnaut S, Roos C, Zinner D (2014) The influence of social systems on patterns of mitochondrial DNA variation in baboons. Int J Primatol 35:210–225

    Article  CAS  PubMed  Google Scholar 

  • Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS One 11:e0154845

    Article  PubMed  PubMed Central  Google Scholar 

  • Lacy RC, Sherman PW (1983) Kin recognition by phenotype matching. Am Sci 121:489–512

    Google Scholar 

  • Langergraber KE (2012) Cooperation among kin. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) Evolution of primate societies. University of Chicago Press, Chicago, pp 491–513

    Google Scholar 

  • Langos D, Kulik L, Mundry R, Widdig A (2013) The impact of paternity on male-infant association in a primate with low paternity certainty. Mol Ecol 22:3638–3651

    Article  PubMed  PubMed Central  Google Scholar 

  • Langos D, Kulik L, Ruiz-Lambides A, Widdig A (2015) Does male care, provided to immature individuals, influence immature fitness in rhesus macaques? PLoS One 10:e013784

    Article  Google Scholar 

  • Lonsdorf EV, Ross SR (2012) Socialization and development of behavior. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) Evolution of primate societies. University of Chicago Press, Chicago, pp 245–268

    Google Scholar 

  • Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative PCR analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835–1844

    Article  CAS  PubMed  Google Scholar 

  • Moscovice LA, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in immatures by male baboons. Behav Ecol Sociobiol 63:1471–1482

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen N, Van Horn RC, Alberts SC, Altmann J (2009) “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol 63:1331–1344

    Article  PubMed  PubMed Central  Google Scholar 

  • Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of "friendships" to female baboons: experimental and observational evidence. Anim Behav 54:599–614

    Article  CAS  PubMed  Google Scholar 

  • Pereira ME, Altmann J (1985) Development of social behavior in free living nonhuman primates. In: Watts ES (ed) Nonhuman primate models for human growth and development. AR Liss, New York, pp 217–309

    Google Scholar 

  • Pereira ME, Fairbanks LA (1993) Immature primates: life history, development and behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 250–266

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists,1st edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Razali NM, Wah YB (2011) Power comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling tests. J Stat Model Anal 2:21–33

    Google Scholar 

  • Sambrook TD, Whiten A, Strum SC (1995) Priority of access and grooming patterns of females in a large and a small group of olive baboons. Anim Behav 50:1667–1682

    Article  Google Scholar 

  • Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420

    Article  PubMed  Google Scholar 

  • Schülke O, Wenzel S, Ostner J (2013) Paternal relatedness predicts the strength of social bonds among female rhesus macaques. PLoS One 8:e59789

    Article  PubMed  PubMed Central  Google Scholar 

  • Silk JB (1987) Social behavior in evolutionary perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 318–329

    Google Scholar 

  • Silk JB (2002) Kin selection in primate groups. Int J Primatol 23:849–875

    Article  Google Scholar 

  • Silk JB, Seyfarth RM, Cheney DL (1999) The structure of social relationships among female savanna baboons in Moremi Reserve, Botswana. Behaviour 36:679–703

    Article  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234

    Article  CAS  PubMed  Google Scholar 

  • Silk JB, Altmann J, Alberts SC (2006a) Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds. Behav Ecol Sociobiol 61:197–204

    Article  Google Scholar 

  • Silk JB, Altmann J, Alberts SC (2006b) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61:183–195

    Article  Google Scholar 

  • 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 Lond B 276:3099–3104

  • Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010a) Female chacma baboons form strong, equitable, and enduring social bonds. Behav Ecol Sociobiol 64:1733–1747

    Article  PubMed  PubMed Central  Google Scholar 

  • Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010b) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361

    Article  CAS  PubMed  Google Scholar 

  • Silk JB, Alberts SC, Altmann J, Cheney DL, Seyfarth RM (2012) Stability of partner choice among female baboons. Anim Behav 83:1511–1518

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith K, Alberts SC, Altmann J (2003) Wild female baboons bias their social behaviour towards paternal half-sisters. Proc R Soc Lond B 270:503–510

    Article  Google Scholar 

  • Smuts BB (1985) Sex and friendships in baboons. Transaction Publishers, Piscataway

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits L, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Hooff JARAM, van Schaik CP (1992) Cooperation in competition: the ecology of primate bonds. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 357–389

    Google Scholar 

  • Van Horn RC, Altmann J, Alberts SC (2008) Can’t get there from here: inferring kinship from pairwise genetic relatedness. Anim Behav 75:1173–1180

    Article  Google Scholar 

  • van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evo Anthropol 5:152–156

  • Widdig A (2007) Paternal kin discrimination: the evidence and likely mechanisms. Biol Rev 82:319–334

    Article  PubMed  Google Scholar 

  • Widdig A, Nurenber P, Krawczak M, Streich WJ, Bercovitch FB (2001) Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. P Natl Acad Sci USA 98:13769–13773

    Article  CAS  Google Scholar 

  • Widdig A, Nurenberg P, Krawczak M, Streich WJ, Bercovitch FB (2002) Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139:371–391

    Article  Google Scholar 

  • Widdig A, Bercovitch FB, Streich WJ, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc Lond B 271:819–826

    Article  Google Scholar 

  • Widdig A, Jurgen S, Nurnberg P, Croucher PJP, Bercovich FB, Krawczak M (2006) Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behav Ecol Sociobiol 61:205–214

    Article  Google Scholar 

  • Widdig A, Langos D, Kulik L (2016) Sex differences in kin bias at maturation: male rhesus macaques prefer paternal kin prior to natal dispersal. Am J Primatol 78:78–91

    Article  PubMed  Google Scholar 

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Acknowledgments

The research was sponsored by the Ministry of Science and Technology of Kenya, the National Museums of Kenya, and the Institute of Primate Research, Nairobi. We are extremely grateful to J. Zeitz for support of the project research on Segera Ranch, and to Ngali ole Resin Lenguya, Patrick Leparleen, Redman Lodungokiok, the staff of ADC Mutara and Segera Ranch, and the residents of Thome B for their important assistance throughout the study. We are also grateful for the contributions from the National Science Foundation BCS-1028750, the L.S.B. Leakey Foundation, and the Fulbright (IIE) Foundation and the Center for Human Evolutionary Studies (Rutgers University). Layon Lenguya assisted significantly in the collection of data. In addition, Mohammed Boru, Lisa Danish, and Nancy Moinde made important contributions throughout the data collection period. We thank Francis Ngasike Kokoi and Anne Nakaredi for their assistance to maintaining the field site. We thank Mary Kelaita for her help with the genetic analysis and John Snyder for his help with the statistical analysis. We appreciate the helpful comments made by Anja Widdig, Robert Scott, and Lee Cronk on this manuscript and contributions made by the reviewers.

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Authors and Affiliations

  1. Department of Anthropology, University of Missouri, 1205 University Place, Columbia, MO, 65203, USA

    Emily C. Lynch & Robert F. Lynch

  2. Department of Anthropology, University of Texas at Austin, 2201 Speedway C3200, Austin, TX, 78712, USA

    Anthony Di Fiore

  3. Department of Anthropology, Rutgers University, 131 George St, New Brunswick, NJ, 08901, USA

    Ryne A. Palombit

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  1. Emily C. Lynch
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Correspondence to Emily C. Lynch.

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Funding

ECL has received funding from the National Science Foundation BCS-1028750, the L.S.B. Leakey Foundation, the Fulbright (IIE) Foundation, and the Center for Human Evolutionary Studies (Rutgers University).

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed (Kenyan Ministry of Education, Science and Technology: MOEST 13/001/29C 120).

Data availability

The datasets analyzed during the current study can be made available from the corresponding author on reasonable request.

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Communicated by A. Widdig

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Lynch, E.C., Di Fiore, A., Lynch, R.F. et al. Fathers enhance social bonds among paternal half-siblings in immature olive baboons (Papio hamadryas anubis). Behav Ecol Sociobiol 71, 120 (2017). https://doi.org/10.1007/s00265-017-2336-y

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  • DOI: https://doi.org/10.1007/s00265-017-2336-y

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