Behavioral Ecology and Sociobiology

, Volume 64, Issue 5, pp 769–781 | Cite as

More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons

  • Elise HuchardEmail author
  • Alexandra Alvergne
  • Delphine Féjan
  • Leslie A. Knapp
  • Guy Cowlishaw
  • Michel Raymond
Original Paper


In mammals, fathers are facultative caretakers, and male care is expected to evolve only if it is directed towards related young. Yet, in several promiscuous primate societies, males seem to care for infants despite a presumably low paternity confidence. In cercopithecines, cohesive associations (‘friendships’) between a lactating female and an adult male are frequent and provide the female and her infant with protection against various sources of aggression, including infanticide. However, the benefits gained by males through such relationships remain unclear, in part, because the relatedness between males and their protected infants has rarely been examined. Moreover, little is known about the nature of the cues underlying kin discrimination by males in societies where females mate polyandrously. In this study, we combine behavioural and genetic data from wild chacma baboons (Papio ursinus) in Namibia to investigate (1) whether males are related to their friend’s infant and (2) whether similarity between the major histocompatibility complex (MHC) genotype of males and infants (potentially perceived through odour phenotype) favours the establishment of friendships. We first show that males share close genetic ties with their friend’s infants, most often by having sired the infant. Secondly, we find that male–infant MHC (Class II–DRB) similarity, in contrast to paternity, does not predict male–infant associations. Overall, our results clarify the nature of the evolutionary benefits gained by males in these heterosexual associations, which can be considered as true paternal care. However, the proximate mechanisms underlying paternity recognition remain to be identified.


Kin selection Primates Infanticide Paternal investment Papio ursinus MHC 



We thank N. Camara, H. Kelstrup, L. De Raad, R. Fleming, J. Kamps, H. Marshall, H. Peck and A. King for their assistance in the field. We are also grateful to S. Funk, A. Randall, A. Dillestone, H. Marshall, C. Staples, J. Osborn and M. Weill for their help with labwork and J. Wang and A. King for their help with parentage analysis and relatedness calculations. We thank the Swart family (2000–2006) and the Ministry of Lands and Resettlement (2006–2007) for their permission to work at Tsaobis Leopard Park, the Gobabeb Training and Research Centre for affiliation, and the Ministry of Environment and Tourism for their research permission in Namibia. Our capture and processing protocols were assessed and approved by the Ethics Committee of the Zoological Society of London. We also confirm that we have adhered to the Guidelines for the Use of Animals in Behavioural Research and Teaching (Animal Behaviour 2006, 71:245–253) and the legal requirements of the country (Namibia) in which the work was carried out. This work was funded by a Natural Environment Research Council (UK) Project Grant and Advanced Fellowship awarded to GC, a Ministère de l’Education et de la Recherche (France) Studentship awarded to EH, and a Royal Society International Travel Grant awarded to both GC and EH. This paper is a publication of the ZSL Institute of Zoology’s Tsaobis Baboon Project. Contribution ISEM 2009-125.

Supplementary material

265_2009_894_MOESM1_ESM.doc (54 kb)
S1 Genetic analyses (DOC 54 kb)
265_2009_894_MOESM2_ESM.doc (56 kb)
Table S2 Characteristics of the 17 loci used for parentage analyses, together with the test results for deviation from Hardy–Weinberg equilibrium (using exact U score tests). Ho observed heterozygosity, He expected heterozygosity, NS non-significant, ***p < 0.001 (DOC 56 kb)
265_2009_894_MOESM3_ESM.doc (36 kb)
Table S3 Demographic composition of the six baboon groups sampled for genetics (DOC 37 kb)
265_2009_894_MOESM4_ESM.doc (32 kb)
Table S4 Assignment of male friends as natal or non-natal in their current troop of residence. All the males listed were already present in the troop at the start of this study. Residency status is defined by the presence in the group for more than a year. See text S1 for details regarding assignments based on genetic data (when demographic information is missing) (DOC 31 kb)
265_2009_894_MOESM5_ESM.doc (122 kb)
Figure S5 Distributions of pairwise relatedness (TL) between juveniles and females (DOC 122 kb)


  1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:27–265CrossRefGoogle Scholar
  2. Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge MAGoogle Scholar
  3. Alvergne A, Faurie C, Raymond M (2009) Father–offspring resemblance predicts paternal investment in humans. Anim Behav 78:61–69CrossRefGoogle Scholar
  4. Bercovitch FB (1991) Mate selection, consortship formation, and reproductive tactics in adult female savanna baboons. Primates 32:437–452CrossRefGoogle Scholar
  5. Birkhead TR, Møller AP (1996) Monogamy and sperm competition in birds. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, Oxford, pp 323–343Google Scholar
  6. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999) Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups—defence pattern, paternity and sexual behaviour. Behav Ecol Sociobiol 46:350–356CrossRefGoogle Scholar
  7. Brown JL, Eklund A (1994) Kin recognition and the major histocompatibility complex—an integrative review. Am Nat 143:435–461CrossRefGoogle Scholar
  8. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181CrossRefPubMedGoogle Scholar
  9. Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103CrossRefGoogle Scholar
  10. Chapais B (1986) Why do adult male and female rhesus monkeys affiliate during the birth season? In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior, and biology. State University of New York Press, Albany, pp 173–200Google Scholar
  11. Charpentier MJE, Boulet M, Drea CM (2008) Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Mol Ecol 17:3225–3233CrossRefPubMedGoogle Scholar
  12. Cheney DL, Seyfarth RM (2007) Baboon metaphysics—the evolution of a social mind. The University of Chicago Press, ChicagoGoogle Scholar
  13. Clarke PMR, Henzi SP, Barrett L (2009) Sexual conflict in chacma baboons, Papio hamadryas ursinus: absent males select for proactive females. Anim Behav 77:1217–1225CrossRefGoogle Scholar
  14. Cowlishaw G (1999) Ecological and social determinants of spacing behaviour in desert baboon groups. Behav Ecol Sociobiol 45:67–77CrossRefGoogle Scholar
  15. Gilad Y, Wiebe V, Przeworski M, Lancet D, Pääbo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biology 2:120–125CrossRefGoogle Scholar
  16. Havlicek J, Roberts C (2009) MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34:497–512CrossRefPubMedGoogle Scholar
  17. Higham JP, Semple S, MacLarnon AM, Heistermann M, Ross C (2009) Female reproductive signaling, and male mating behavior, in the olive baboon. Horm Behav 55:60–67CrossRefPubMedGoogle Scholar
  18. 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
  19. Hinde RA, Proctor LP (1977) Changes in the relationships of captive rhesus monkeys on giving birth. Behaviour 61:304–321CrossRefGoogle Scholar
  20. Huchard E, Cowlishaw G, Raymond M, Weill M, Knapp LA (2006) Molecular study of Mhc-DRB in wild chacma baboons reveals high variability and evidence for trans-species inheritance. Immunogenetics 58:805–816CrossRefPubMedGoogle Scholar
  21. Huchard E, Weill M, Cowlishaw G, Raymond M, Knapp LA (2008) Polymorphism, haplotype composition, and selection in the Mhc-DRB of wild baboons. Immunogenetics 60:585–598CrossRefPubMedGoogle Scholar
  22. 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. Proceedings of the Royal Society, Series B 276:1889–1897CrossRefGoogle Scholar
  23. Johnstone RA (1997) Recognition and the evolution of distinctive signatures: when does it pay to reveal identity? Proc R Soc Lond B 264:1547–1553CrossRefGoogle Scholar
  24. Kahumbu P, Eley RM (1991) Teeth emergence in wild olive baboons in Kenya and formulation of a dental schedule for ageing wild baboon populations. Am J Primatol 23:1–9CrossRefGoogle Scholar
  25. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–2006CrossRefPubMedGoogle Scholar
  26. Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Parental care in mammals. Plenum, New York, pp 347–387Google Scholar
  27. Kwak J, Willse A, Matsumura K, Opiekun MC, Yi W, Preti G, Yamazaki K, Beauchamp GK (2008) Genetically-based olfactory signatures persist despite dietary variation. PloS One 3:10CrossRefGoogle Scholar
  28. Lacy RC, Sherman PW (1983) Kin recognition by phenotype matching. Am Nat 121:489–512CrossRefGoogle Scholar
  29. Lehmann J, Fickenscher G, Boesch C (2007) Kin biased investment in wild chimpanzees. Behaviour 143:931–955CrossRefGoogle Scholar
  30. 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
  31. Manning CJ, Wakeland EK, Potts WK (1992) Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360:581–583CrossRefPubMedGoogle Scholar
  32. Mason JH (1994) Mating patterns, mate choice, and birth season heterosexual relationships in free-ranging rhesus macaques. Primates 35:417–433CrossRefGoogle Scholar
  33. Mateo JM (2002) Kin-recognition abilities and nepotism as a function of sociality. Proc R Soc Lond B 269:721–727CrossRefGoogle Scholar
  34. 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). Les Comptes Rendus de l’Académie des Sciences de Paris. Life Sci 324:601–610Google Scholar
  35. 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 63:1471–1482CrossRefPubMedGoogle Scholar
  36. Mundry R, Nunn CL (2009) Stepwise model fitting and statistical inference: turning noise into signal pollution. Am Nat 173:119–123CrossRefPubMedGoogle Scholar
  37. Neff BD, Sherman PW (2005) In vitro fertilisation reveals offspring recognition via self-referencing in a fish with paternal care and cuckoldry. Ethology 111:425–438CrossRefGoogle Scholar
  38. 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 63:1331–1344CrossRefGoogle Scholar
  39. 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, CambridgeGoogle Scholar
  40. 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, pp 367–412Google Scholar
  41. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of “friendship” to female baboons: experimental and observational evidence. Anim Behav 54:599–614CrossRefPubMedGoogle Scholar
  42. 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
  43. Paul A, Kuester J, Arnemann J (1996) The sociobiology of male–infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170CrossRefGoogle Scholar
  44. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21CrossRefGoogle Scholar
  45. Perrone MJ, Zaret TM (1979) Parental care patterns of fishes. Am Nat 113:351–361CrossRefGoogle Scholar
  46. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. SpringerGoogle Scholar
  47. Price EC (1990) Infant carrying as a courtship strategy of breeding male cotton-top tamarins. Anim Behav 40:784–786CrossRefGoogle Scholar
  48. Ransom TW, Ransom BS (1971) Adult male–infant relations among baboons (Papio anubis). Folia Primatol 16:179–195CrossRefPubMedGoogle Scholar
  49. Seyfarth RM (1978) Social relationships among adult male and female baboons. II. Behaviour throughout the female reproductive cycle. Behaviour 64:227–247CrossRefGoogle Scholar
  50. Smuts BB (1985) Sex and friendship in baboons. Aldine, New YorkGoogle Scholar
  51. Strum SC (1984) Why males use infants. In: Taub DM (ed) Primate paternalism. Van Nostrand Reinhold Inc., New York, pp 146–185Google Scholar
  52. Takahata Y (1982) Social relations between adult males and females of Japanese monkeys in the Arashiyama B troop. Primates 23:1–23CrossRefGoogle Scholar
  53. Team RDC (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  54. Todrank J, Heth G, Johnston RE (1998) Kin recognition in golden hamsters: evidence for kinship odour. Anim Behav 55:377–386CrossRefPubMedGoogle Scholar
  55. Trivers RL (1972) Parental investment and sexual selection. In: Campbell P (ed) Sexual selection and the descent of man. Heinemann, London, pp 136–179Google Scholar
  56. van Schaik CP, Janson CH (2000) Infanticide by males and its implications. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  57. 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
  58. van Schaik CP, Paul A (1997) Male care in primates: does it ever reflect paternity? Evol.Anthropol 5:152–156Google Scholar
  59. Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979CrossRefPubMedGoogle Scholar
  60. Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153CrossRefPubMedGoogle Scholar
  61. 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
  62. Wetton JH, Carter RE, Parkin DT, Walters D (1987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147–149CrossRefPubMedGoogle Scholar
  63. Widdig A (2007) Paternal kin discrimination: the evidence and likely mechanisms. Biol Rev 82:319–334CrossRefPubMedGoogle Scholar
  64. Willse A, Kwak J, Yamazaki K, Preti G, Wahl JH, Beauchamp GK (2006) Individual odortypes: interaction of MHC and background genes. Immunogenetics 58:967–982CrossRefPubMedGoogle Scholar
  65. Yamazaki K, Beauchamp GK (2007) Genetic basis for MHC-dependent mate choice. Adv Genet 59:130–145Google Scholar
  66. Yamazaki K, Beauchamp GK, Curran M, Bard J, Boyse EA (2000) Parent–progeny recognition as a function of MHC odortype identity. Proc Natl Acad Sci USA 97:10500–10502CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Elise Huchard
    • 1
    • 2
    • 4
    Email author
  • Alexandra Alvergne
    • 1
    • 5
  • Delphine Féjan
    • 1
  • Leslie A. Knapp
    • 3
  • Guy Cowlishaw
    • 2
  • Michel Raymond
    • 1
  1. 1.CNRS–Institut des Sciences de l’Evolution de MontpellierUniversité Montpellier IIMontpellierFrance
  2. 2.Institute of ZoologyZoological Society of LondonLondonUK
  3. 3.Department of Biological AnthropologyUniversity of CambridgeCambridgeUK
  4. 4.Abteilung Verhaltensökologie und SoziobiologieDeutsches PrimatenzentrumGöttingenGermany
  5. 5.Human Evolutionary Ecology Group, Department of AnthropologyUniversity College LondonLondonUK

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