Behavioral Ecology and Sociobiology

, Volume 70, Issue 5, pp 761–775

Stability and strength of male-female associations in a promiscuous primate society

Original Article

Abstract

Close associations between adult males and lactating females occur in several promiscuous primate species. Benefits gained by males from such bonds may include increases in offspring fitness through paternal effort (the “mate-then-care” hypothesis) and/or subsequent mating opportunities with the female (the “care-then-mate” hypothesis). Heterosexual friendships between males and females have been described as tightly linked to the presence of a dependent infant, but few studies have investigated whether these associations may be longer, starting before an infant birth and lasting after its independence, and whether they may vary in strength across time and dyads. We investigated the stability and strength of heterosexual bonds in two groups of wild chacma baboons (Papio ursinus) to test whether male-female associations (1) last from offspring conception to independence, as expected under the mate-then-care hypothesis, (2) last after maternal cycling resumption and increase male mating success, as expected under the care-then-mate hypothesis, and (3) vary in strength depending on female reproductive state, age and rank. Our results show that most male-female bonds were already present at offspring conception, were maintained during pregnancy and lactation and disappeared when mothers resumed cycling. Moreover, heterosexual bonds were most intense during early lactation and for high-ranking females, and did not predict subsequent mating activity. Those findings favour the mate-then-care hypothesis, and confirm that male paternity assessment may, at least partially, rely on mating history. Overall, stable heterosexual friendships exist outside early lactation and last longer than previously thought, suggesting that male-female bonds could play an important and under-appreciated role on the social structure of groups in promiscuous primate societies.

Significance statement

Stable male-female bonds are rare in promiscuous mammals. Baboons are unusual in this respect: tight friendships have been described between adult males and lactating females and may protect infants against infanticide, but few studies have investigated whether these associations may start before an infant’s birth, or extend after its nutritional independence. We explored the stability and strength of heterosexual relationships in the chacma baboon, and found that friendships start before or at infant’s conception, are maintained throughout pregnancy, strengthen during lactation and disappear when mothers resume cycling. Such pattern of association suggests that male-female bonds represent paternal effort, and may arise from sexual activity before and during the conceptive cycle. Most females appear permanently associated with one male regardless of their reproductive state, suggesting that heterosexual bonds play an important, and under-appreciated, role in structuring the social organization of baboon societies.

Keywords

Friendship Male-female association Paternal care Mating success Chacma baboon Papio ursinus 

Supplementary material

265_2016_2100_MOESM1_ESM.docx (287 kb)
ESM 1(DOCX 286 kb)

References

  1. Agoramoorthy G, Mohnot SM, Sommer V, Srivastavz A (1988) Abortions in free ranging Hanuman langurs (Presbytis entellus)—a male induced strategyGoogle Scholar
  2. Albers PCH, de Vries H (2001) Elo-rating as a tool in the sequential estimation of dominance strengths. Anim Behav 61:489–495CrossRefGoogle Scholar
  3. Alberts SC, Altmann J (1995) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306CrossRefGoogle Scholar
  4. Alberts SC, Sapolsky RM, Altmann J (1992) Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav 26:167–178CrossRefPubMedGoogle Scholar
  5. Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277CrossRefGoogle Scholar
  6. Altmann SA (1973) The pregnancy sign in savannah baboons. J Zoo Anim Med 4:8–12CrossRefGoogle Scholar
  7. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  8. Altmann J (1980) Baboon mothers and infants. Harvard University Press, CambridgeGoogle Scholar
  9. Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409CrossRefPubMedGoogle Scholar
  10. 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 281:20141261CrossRefPubMedPubMedCentralGoogle Scholar
  11. Aureli F, Yates K (2009) Distress prevention by grooming others in crested black macaques. Biol Lett 6:27–29CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bales KB (1980) Cumulative scaling of paternalistic behavior in primates. Am Nat 454–461Google Scholar
  13. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7, https://cran.rproject.org/web/packages/lme4/index.html
  14. Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2005) The effect of new alpha males on female stress in free-ranging baboons. Anim Behav 69:1211–1221CrossRefGoogle Scholar
  15. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236CrossRefPubMedGoogle Scholar
  16. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181CrossRefPubMedGoogle Scholar
  17. Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103CrossRefGoogle Scholar
  18. Cacioppo JT, Hawkley LC (2003) Social isolation and health, with an emphasis on underlying mechanisms. Perspect Biol Med 46:S39–S52CrossRefPubMedGoogle Scholar
  19. Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci U S A 106:13850–13853CrossRefPubMedPubMedCentralGoogle Scholar
  20. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008) Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci U S A 105:1988–1992CrossRefPubMedPubMedCentralGoogle Scholar
  21. Cheney DL, Silk JB, Seyfarth RM (2012) Evidence for intrasexual selection in wild female baboons. Anim Behav 84:21–27CrossRefPubMedPubMedCentralGoogle Scholar
  22. Colmenares F, Gomendio M (1988) Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons. Folia Primatol 50:157–174CrossRefPubMedGoogle Scholar
  23. Cowlishaw G (1997) Refuge use and predation risk in a desert baboon population. Anim Behav 54:241–253CrossRefPubMedGoogle Scholar
  24. Cushing BS, Carter CS (2000) Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles. Horm Behav 37:49–56CrossRefPubMedGoogle Scholar
  25. Daspre A, Heistermann M, Hodges JK, Lee PC, Rosetta L (2009) Signals of female reproductive quality and fertility in colony-living baboons (Papio h. anubis) in relation to ensuring paternal investment. Am J Primatol 71:529–538CrossRefPubMedGoogle Scholar
  26. DeVries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407CrossRefPubMedGoogle Scholar
  27. Ellis JJ, Maclarnon AM, Heistermann M, Semple S (2011) The social correlates of self-directed behaviour and faecal glucocorticoid levels among adult male olive baboons (Papio hamadryas anubis) in Gashaka-Gumti National Park, Nigeria. Afr Zool 46:302–308CrossRefGoogle Scholar
  28. Engh AL, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL (2006) Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons. Anim Behav 71:1227–1237CrossRefGoogle Scholar
  29. Feldman R, Zagoory-Sharon O, Weisman O, Schneiderman I, Gordon I, Maoz R, Shalev I, Ebstein RP (2012) Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 Genes. Biol Psychiat 72:175–181CrossRefPubMedGoogle Scholar
  30. Frere CH, Krutzen M, Mann J, Connor RC, Bejder L, Sherwin WB (2010) Social and genetic interactions drive fitness variation in a free-living dolphin population. Proc Natl Acad Sci U S A 107:19949–19954CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gilbert C, Gillman J (1952) Pregnancy in the baboon (Papio ursinus). S Afr J Med Sci 16:115–124PubMedGoogle Scholar
  32. Grewen KM, Girdler SS, Amico J, Light KC (2005) Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosom Med 67:531–538CrossRefPubMedGoogle Scholar
  33. Handley LJL, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578CrossRefGoogle Scholar
  34. Higham JP, Heistermann M, Ross C, Semple S, MacLarnon A (2008) The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates 49:295–299CrossRefPubMedGoogle Scholar
  35. Hinde RA, Atkinson S (1970) Assessing the role of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. Anim Behav 18:169–176CrossRefGoogle Scholar
  36. Hinde RA, Proctor LP (1977) Changes in the relationships of captive rhesus monkeys on giving birth. Behaviour 61:304–321CrossRefGoogle Scholar
  37. Holt-Lunstad J, Smith TB, Bradley Layton J (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7:859CrossRefGoogle Scholar
  38. Huchard E, Cowlishaw G (2011) Female-female aggression around mating: an extra cost of sociality in a multimale primate society. Behav Ecol 22:1003–1011CrossRefGoogle Scholar
  39. Huchard E, Courtiol A, Benavides JA, Knapp LA, Raymond M, Cowlishaw G (2009) Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings. Proc R Soc Lond B 276:1889–1897CrossRefGoogle Scholar
  40. Huchard E, Alvergne A, Fejan D, Knapp LA, Cowlishaw G, Raymond M (2010) More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons. Behav Ecol Sociobiol 64:769–781CrossRefGoogle Scholar
  41. 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 24:229–236CrossRefGoogle Scholar
  42. Kaplan BS, O’Riain MJ, van Eeden R, King AJ (2011) A low-cost manipulation of food resources reduces spatial overlap between baboons (Papio ursinus) and humans in conflict. Int J Primatol 32:1397–1412CrossRefGoogle Scholar
  43. Kerhoas D, Perwitasari-Farajallah D, Agil M, Widdig A, Engelhardt A (2014) Social and ecological factors influencing offspring survival in wild macaques. Behav Ecol 25:1164–1172CrossRefPubMedPubMedCentralGoogle Scholar
  44. King AJ, Douglas CMS, Huchard E, Isaac NJB, Cowlishaw G (2008) Dominance and affiliation mediate despotism in a social primate. Curr Biol 18:1833–1838CrossRefPubMedGoogle Scholar
  45. Kulik L, Muniz L, Mundry R, Widdig A (2012) Patterns of interventions and the effect of coalitions and sociality on male fitness. Mol Ecol 21:699–714CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lemasson A, Palombit RA, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035CrossRefGoogle Scholar
  47. Machanda ZP, Gilby IC, Wrangham RW (2013) Male-female association patterns among free-ranging chimpanzees (Pan troglodytes schweinfurthii). Int J Primatol 34:917–938CrossRefGoogle Scholar
  48. Manson JH (1994) Mating patterns, mate choice, and birth season heterosexual relationships in free-ranging rhesus macaques. Primates 35:417–433CrossRefGoogle Scholar
  49. Massen JJM, Overduin-de Vries AM, de Vos-Rouweler AJM, Spruijt BM, Doxiadis GGM, Sterck EHM (2012) Male mating tactics in captive rhesus macaques (Macaca mulatta): the influence of dominance, markets, and relationship quality. Int J Primatol 33:73–92CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ménard N, von Segesser F, Scheffrahn W, Pastorini J, Vallet D, Gaci B, Martin RD, Gautier-Hion A (2001) Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus). CR Acad Sci III-Vie 324:601–610CrossRefGoogle Scholar
  51. Moscovice LR, Ziegler TE (2012) Peripheral oxytocin in female baboons relates to estrous state and maintenance of sexual consortships. Horm Behav 62:592–597CrossRefPubMedPubMedCentralGoogle Scholar
  52. Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol 63:1471–1482CrossRefPubMedPubMedCentralGoogle Scholar
  53. Moscovice LR, Di Fiore A, Crockford C, Kitchen DM, Wittig R, Seyfarth RM, Cheney DL (2010) Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. Anim Behav 79:1007–1015CrossRefGoogle Scholar
  54. Mundry R, Nunn CL (2009) Stepwise model fitting and statistical inference: turning noise into signal pollution. Am Nat 173:119–123CrossRefPubMedGoogle Scholar
  55. Neumann C, Duboscq J, Dubuc C, Ginting A, Irwan AM, Agil M, Widdig A, Engelhardt A (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921CrossRefGoogle Scholar
  56. 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 63:1331–1344CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ostner J, Vigilant L, Bhagavatula J, Franz M, Schülke O (2013) Stable heterosexual associations in a promiscuous primate. Anim Behav 86:623–631CrossRefGoogle Scholar
  58. Palombit RA (1999) Infanticide and the evolution of pair bonds in nonhuman primates. Evol Anthropol 7:117–129CrossRefGoogle Scholar
  59. Palombit RA (2000) Infanticide and the evolution of male-female bonds in animals. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 239–268CrossRefGoogle Scholar
  60. Palombit RA (2003) Male infanticide in wild savanna baboons: adaptive significance and intraspecific variation. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 367–412Google Scholar
  61. Palombit RA (2012) Infanticide: male strategies and female counterstrategies. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JA (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 432–468Google Scholar
  62. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of “friendships” to female baboons: experimental and observational evidence. Anim Behav 54:599–614CrossRefPubMedGoogle Scholar
  63. Palombit RA, Cheney DL, Fisher J, Johnson S, Rendall D, Seyfarth RM, Silk JB (2000) Male infanticide and defense of infants in chacma baboons. In: van Schaik C, Janson C (eds) Infanticide by males and its implications, Cambridge. Cambridge, pp 123–152Google Scholar
  64. Palombit RA, Cheney DL, Seyfarth RM (2001) Female-female competition for male “friends” in wild chacma baboons, Papio cynocephalus ursinus. Anim Behav 61:1159–1171CrossRefGoogle Scholar
  65. Paul A, Kuester J, Arnemann J (1996) The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170CrossRefGoogle Scholar
  66. Pereira ME (1983) Abortion following the immigration of an adult male baboon (Papio cynocephalus). Am J Primatol 4:93–98CrossRefGoogle Scholar
  67. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer, New YorkCrossRefGoogle Scholar
  68. R Core Development Team (2015) R: A language and environment for statistical computing. Vienna, Austria, http://www.r-project.org/
  69. Roberts EK, Lu A, Bergman TJ, Beehner JC (2012) A Bruce effect in wild geladas. Science 335:1222–1225CrossRefPubMedGoogle Scholar
  70. Rosal MC, King J, Ma Y, Reed GW (2004) Stress, social support, and cortisol: inverse associations? Behav Med 30:11–21CrossRefPubMedGoogle Scholar
  71. Seyfarth RM (1976) Social relationships among adult female baboons. Anim Behav 24:917–938CrossRefGoogle Scholar
  72. Seyfarth RM (1978) Social relationships among adult male and female baboons. II Behaviour throughout the female reproductive cycle. Behaviour 64:227–247CrossRefGoogle Scholar
  73. Silk JB (2007a) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559CrossRefGoogle Scholar
  74. Silk JB (2007b) Social components of fitness in primate groups. Science 317:1347–1351CrossRefPubMedGoogle Scholar
  75. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1232CrossRefPubMedGoogle Scholar
  76. 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 276:3099–3104CrossRefGoogle Scholar
  77. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361CrossRefPubMedGoogle Scholar
  78. Smith AS, Ågmo A, Birnie AK, French JA (2010) Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Horm Behav 57:255–262CrossRefPubMedPubMedCentralGoogle Scholar
  79. Smuts BB (1985) Sex and friendship in baboons. Aldine, New yorkGoogle Scholar
  80. Smuts BB, Gubernick DJ (1992) Male-infant relationships in nonhuman primates: paternal investment or mating effort? In: Hewlett BS (ed) Father-child relations: cultural and biosocial contexts. Aldine de Gruyter, New York, pp 1–30Google Scholar
  81. Snowdon CT, Pieper BA, Boe CY, Cronin KA, Kurian AV, Ziegler TE (2010) Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins. Horm Behav 58:614–618CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stanton MA, Mann J (2012) Early social networks predict survival in wild bottlenose dolphins. PLoS One 7:e47508CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  84. Uchino BN (2006) Social support and health: a review of physiological processes potentially underlying links to disease outcomes. J Behav Med 29:377–387CrossRefPubMedGoogle Scholar
  85. van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology: the behavioral ecology of humans and other mammals. Blackwell Scientific, Oxford, pp 195–218Google Scholar
  86. van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male-female association in primates. Proc R Soc Lond B 264:1687–1694CrossRefGoogle Scholar
  87. van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evol Anthropol 5:152–156CrossRefGoogle Scholar
  88. van Schaik CP, van Noordwijk MA (1989) The special role of male Cebus monkeys in predation avoidance and its effect on group composition. Behav Ecol Sociobiol 24:265–276CrossRefGoogle Scholar
  89. Weingrill T (2000) Infanticide and the value of male-female relationships in mountain chacma baboons. Behaviour 137:337–359CrossRefGoogle Scholar
  90. Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP (2003) Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140:405–427CrossRefGoogle Scholar
  91. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189CrossRefPubMedGoogle Scholar
  92. Widdig A (2007) Paternal kin discrimination: the evidence and likely mechanisms. Biol Rev 82:319–334CrossRefPubMedGoogle Scholar
  93. Williams JR, Insel TR, Harbaugh CR, Carter CS (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247–250CrossRefPubMedGoogle Scholar
  94. Witt DM, Carter CS, Walton DM (1990) Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol Biochem Behav 37:63–69CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Centre d’Ecologie Fonctionnelle et Evolutive, Unité Mixte de Recherche 5175, Centre National de la Recherche ScientifiqueMontpellier Cedex 5France
  2. 2.Institut des Sciences de l’Evolution de MontpellierUniversité de Montpellier, Place Eugène BataillonMontpellier Cedex 5France
  3. 3.Institute of ZoologyThe Zoological Society of LondonLondonUK

Personalised recommendations