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Same-sex sociosexual behaviour is widespread and heritable in male rhesus macaques

Nature Ecology & Evolution volume 7, pages 1287–1301 (2023)Cite this article

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Abstract

Numerous reports have documented the occurrence of same-sex sociosexual behaviour (SSB) across animal species. However, the distribution of the behaviour within a species needs to be studied to test hypotheses describing its evolution and maintenance, in particular whether the behaviour is heritable and can therefore evolve by natural selection. Here we collected detailed observations across 3 yr of social and mounting behaviour of 236 male semi-wild rhesus macaques, which we combined with a pedigree dating back to 1938, to show that SSB is both repeatable (19.35%) and heritable (6.4%). Demographic factors (age and group structure) explained SSB variation only marginally. Furthermore, we found a positive genetic correlation between same-sex mounter and mountee activities, indicating a common basis to different forms of SSB. Finally, we found no evidence of fitness costs to SSB, but show instead that the behaviour mediated coalitionary partnerships that have been linked to improved reproductive success. Together, our results demonstrate that SSB is frequent in rhesus macaques, can evolve, and is not costly, indicating that SSB may be a common feature of primate reproductive ecology.

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Fig. 1: Prevalence and distribution of mounting behaviour.
Fig. 2: Repeatability and heritability of same-sex mounting behaviour.
Fig. 3: Correlations of mounting behaviours.

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Data availability

Data generated and analysed in this study are included as Supplementary Information (listed below). Full datasets are available from https://github.com/JacksonClive/Same-sex-sociosexual-behaviour-is-widespread-and-heritable-in-male-rhesus-macaques/. Due to the lengthy runtimes of some of our MCMC GLMMs, we have provided these model outputs as stored R objects (.rds). Monkey ID codes have been anonymized in accordance with CPRC policy. Descriptions for each supplementary data file are provided in Supplementary Information.

Code availability

All code is available from https://github.com/JacksonClive/Same-sex-sociosexual-behaviour-is-widespread-and-heritable-in-male-rhesus-macaques/. Details of the analysis pipeline are provided in the README.md.

References

  1. Sommer, V. & Vasey, P. L. Homosexual Behaviour in Animals: An Evolutionary Perspective (Cambridge Univ. Press, 2006).

  2. Bailey, J. M. et al. Sexual orientation, controversy and science. Psychol. Sci. Public Interest 17, 45–101 (2016).

    Article  PubMed  Google Scholar 

  3. Bailey, N. W. & Zuk, M. Same-sex sexual behavior and evolution. Trends Ecol. Evol. 24, 439–446 (2009).

    Article  PubMed  Google Scholar 

  4. Scharf, I. & Martin, O. Y. Same-sex sexual behavior in insects and arachnids: prevalence, causes and consequences. Behav. Ecol. Sociobiol. 67, 1719–1730 (2013).

    Article  Google Scholar 

  5. Sandel, A. A. & Reddy, R. B. Sociosexual behaviour in wild chimpanzees occurs in variable contexts and is frequent between same-sex partners. Behaviour 158, 249–276 (2021).

    Article  Google Scholar 

  6. Altmann, S. A. A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann. N. Y. Acad. Sci. 102, 338–435 (1962).

    Article  CAS  PubMed  Google Scholar 

  7. Fox, E. A. Homosexual behavior in wild Sumatran orangutans (Pongo pygmaeus abelii). Am. J. Primatol. 55, 177–181 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Jiang, T. et al. Homosexual mounting in wild male Tibetan Macaques (Macaca thibetana) at Huangshan, China. Life Sci. J. 10, 3192–3197 (2013).

    Google Scholar 

  9. Vasey, P. L., Leca, J. B., Gunst, N. & VanderLaan, D. P. Female homosexual behavior and inter-sexual mate competition in Japanese macaques: possible implications for sexual selection theory. Neurosci. Biobehav. Rev. 46, 573–578 (2014).

    Article  PubMed  Google Scholar 

  10. Leca, J. B., Gunst, N. & Vasey, P. L. Male homosexual behavior in a free-ranging all-male group of Japanese macaques at Minoo, Japan. Arch. Sex. Behav. 43, 853–861 (2014).

    Article  PubMed  Google Scholar 

  11. Hoskins, J. L., Ritchie, M. G. & Bailey, N. W. A test of genetic models for the evolutionary maintenance of same-sex sexual behaviour. Proc. R. Soc. B. 282, 20150429 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Berger, D. et al. Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior. BMC Evol. Biol. 16, 88 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Burri, A., Spector, T. & Rahman, Q. Common genetic factors among sexual orientation, gender nonconformity and number of sex partners in female twins: implications for the evolution of homosexuality. J. Sex. Med. 12, 1004–1011 (2015).

    Article  PubMed  Google Scholar 

  14. Ganna, A., 23andMe Research Team. et al. Large-scale GWAS reveals insights into the genetic architecture of same-sex sexual behavior. Science 365, eaat7693 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hu, S. H. et al. Discovery of new genetic loci for male sexual orientation in Han population. Cell Discov. 7, 103 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Xue, A. et al. Genome-wide analyses of behavioural traits are subject to bias by misreports and longitudinal changes. Nat. Commun. 12, 20211 (2021).

    Article  CAS  PubMed  Google Scholar 

  17. Xue, C. et al. The population genomics of rhesus macaques (Macaca mulatta) based on whole-genome sequences. Genome Res. 26, 1651–1662 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kanthaswamy, S. et al. Population genetic structure of the Cayo Santiago colony of rhesus macaques (Macaca mulatta). J. Am. Assoc. Lab. Anim. Sci. 56, 396–401 (2017).

    PubMed  PubMed Central  Google Scholar 

  19. Blomquist, G. E. & Brent, L. J. Applying quantitative genetic methods to primate social behavior. Int. J. Primatol. 35, 108–128 (2014).

    Article  PubMed  Google Scholar 

  20. Bailey, J. M., Pillard, R. C., Neale, M. C. & Agyei, Y. Heritable factors influence sexual orientation in women. Arch. Gen. Psychiatry 50, 217–223 (1993).

    Article  CAS  PubMed  Google Scholar 

  21. Carpenter, C. R. Sexual behavior of free ranging rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 33, 113–142 (1941).

    Article  Google Scholar 

  22. Lindburg, D. G. in Primate Behavior: Developments in Field and Laboratory Research Vol. 2. (ed. Rosenblum, L. A.) 1–106 (Academic Press, 1971).

  23. Higham, J. P. et al. Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav. Ecol. 21, 739–746 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Clay, Z. & de Waal, F. B. M. Sex and strife: post-conflict sexual contacts in bonobos. Behaviour 152, 313–334 (2015).

    Article  Google Scholar 

  25. Annicchiarico, G., Bertini, M., Cordoni, G. & Palagi, E. Look at me while having sex! Eye-to-eye contact affects homosexual behaviour in bonobo females. Behaviour 157, 949–970 (2020).

    Article  Google Scholar 

  26. Bonnet, X. et al. A prison effect in a wild population: a scarcity of females induces homosexual behaviors in males. Behav. Ecol. 27, 1206–1215 (2016).

    Article  Google Scholar 

  27. Jankowiak, Ł., Tryjanowski, P., Hetmański, T. & Skórka, P. Experimentally evoked same-sex sexual behaviour in pigeons: better to be in a female-female pair than alone. Sci. Rep. 8, 1654 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Vasey, P. L. & Gauthier, C. Skewed sex ratios and female homosexual activity in Japanese macaques: an experimental analysis. Primates 41, 17–25 (2000).

    Article  PubMed  Google Scholar 

  29. Gordon, T. P. & Bernstein, I. S. Seasonal variation in sexual behavior of all-male rhesus troops. Am. J. Phys. Anthropol. 38, 221–225 (1973).

    Article  CAS  PubMed  Google Scholar 

  30. Han, C. S. & Brooks, R. C. The interaction between genotype and juvenile and adult density environment in shaping multidimensional reaction norms of behaviour. Funct. Ecol. 29, 78–87 (2015).

    Article  Google Scholar 

  31. Grueter, C. C. & Stoinski, T. S. Homosexual behavior in female mountain gorillas: reflection of dominance, affiliation, reconciliation or arousal? PLoS ONE 11, e0154185 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rufo, H. P. & Ottoni, E. B. Anecdotic observations of homosexual behaviour among male capuchin monkeys (Sapajus sp.). Behaviour 158, 89–97 (2020).

    Article  Google Scholar 

  33. Reinhardt, V., Reinhardt, A., Bercovitch, F. B. & Goy, R. W. Does intermale mounting function as a dominance demonstration in rhesus monkeys? Folia Primatol. 47, 55–60 (1986).

    Article  CAS  Google Scholar 

  34. Good, P. I. Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses (Springer, 2000).

  35. de Villemereuil, P. Quantitative genetic methods depending on the nature of the phenotypic trait. Ann. N. Y. Acad. Sci. 1422, 29–47 (2018).

    Article  PubMed  Google Scholar 

  36. Visscher, P. M., Hill, W. G. & Wray, N. R. Heritability in the genomics era – concepts and misconceptions. Nat. Rev. Genet. 9, 255–266 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Watson, K. K. et al. Genetic influences on social attention in free-ranging rhesus macaques. Anim. Behav. 103, 267–275 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ratnu, V. S., Emami, M. R. & Bredy, T. W. Genetic and epigenetic factors underlying sex differences in the regulation of gene expression in the brain. J. Neur. Res. 95, 301–310 (2017).

    Article  CAS  Google Scholar 

  39. Gavrilets, S. & Rice, W. R. Genetic models of homosexuality: generating testable predictions. Proc. R. Soc. B. 273, 3031–3038 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Clive, J., Flintham, E. & Savolainen, V. Understanding same-sex sexual behaviour requires thorough testing rather than reinvention of theory. Nat. Ecol. Evol. 4, 784–785 (2020).

    Article  PubMed  Google Scholar 

  41. Savolainen, V. & Hodgson, J. A. in Encyclopedia of Evolutionary Psychological Science (eds Weekes-Shackelford, V. A. & Shackelford, T. K.) 2325–2532 (Springer, 2016).

  42. Gavrilets, S., Friberg, U. & Rice, W. R. Understanding homosexuality: moving on from patterns to mechanisms. Arch. Sex. Behav. 47, 27–31 (2018).

    Article  PubMed  Google Scholar 

  43. Zietsch, B. P. et al. Genomic evidence consistent with antagonistic pleiotropy may help explain the evolutionary maintenance of same-sex sexual behaviour in humans. Nat. Hum. Behav. 5, 1251–1258 (2021).

    Article  PubMed  Google Scholar 

  44. Hansen, T. F., Pélabon, C. & Houle, D. Heritability is not evolvability. Evol. Biol. 38, 258–277 (2011).

    Article  Google Scholar 

  45. Gervais, L. et al. Pedigree‐free quantitative genetic approach provides evidence for heritability of movement tactics in wild roe deer. J. Evol. Biol. 33, 595–607 (2020).

    Article  PubMed  Google Scholar 

  46. Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).

    Article  PubMed  Google Scholar 

  47. Mesterton-Gibbons, M., Gavrilets, S., Gravner, J. & Akcay, E. Models of coalition or alliance formation. J. Theor. Biol. 274, 187–204 (2011).

    Article  PubMed  Google Scholar 

  48. Neumann, C., Kulik, L., Agil, M., Engelhardt, A. & Widdig, A. Temporal dynamics and fitness consequences of coalition formation in male primates. Proc. R. Soc. B. 289, 20212626 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kirkpatrick, R. C. The evolution of human homosexual behavior. Curr. Anthropol. 41, 385–413 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Vasey, P. L., Rains, D., VanderLaan, D. P., Duckworth, N. & Kovacovsky, S. D. Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships. Behav. Proc. 78, 401–407 (2008).

    Article  CAS  Google Scholar 

  51. Surbeck, M. & Hohmann, G. Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus). Behav. Ecol. Sociobiol. 67, 1767–1780 (2013).

    Article  Google Scholar 

  52. Tokuyama, N. & Furuichi, T. Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba. Anim. Behav. 119, 27–35 (2016).

    Article  Google Scholar 

  53. Moscovice, L. R. et al. Stable and fluctuating social preferences and implications for cooperation among female bonobos at Lui Kotale, Salonga National Park, DRC. Am. J. Phys. Anthropol. 163, 158–172 (2017).

    Article  PubMed  Google Scholar 

  54. Moscovice, L. R. et al. The cooperative sex: sexual interactions among female bonobos are linked to increases in oxytocin, proximity and coalitions. Horm. Behav. 116, 104581 (2019).

    Article  CAS  PubMed  Google Scholar 

  55. Wiszniewski, J., Corrigan, S., Beheregaray, L. B. & Möller, L. M. Male reproductive success increases with alliance size in Indo-Pacific bottlenose dolphins (Tursiops aduncus). J. Ecol. 81, 423–431 (2012).

    Article  Google Scholar 

  56. Smuts, B. B. & Watanabe, J. M. Social relationships and ritualized greetings in adult male baboons (Papio cynocephalus anubis). Int. J. Primatol. 11, 147–172 (1990).

    Article  Google Scholar 

  57. Savulescu, J., Earp, B. D. & Schuklenk, U. Ethics of genetic research on same-sex sexual behaviour. Nat. Hum. Behav. 5, 1123–1124 (2021).

    Article  PubMed  Google Scholar 

  58. Hammack-Aviran, C. et al. LGBTQ+ perspectives on conducting genomic research on sexual orientation and gender identity. Behav. Genet. 52, 246–267 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Egleston, B. L., Dunbrack, R. L. Jr. & Hall, M. J. Clinical trials that explicitly exclude gay and lesbian patients. N. Engl. J. Med. 362, 1054–1055 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Hughes, B. E. Coming out in STEM: factors affecting retention of sexual minority STEM students. Sci. Adv. 4, eaao6373 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Powell, K., Terry, R. & Chen, S. How LGBT+ scientists would like to be included and welcomed in STEM workplaces. Nature 586, 813–817 (2020).

    Article  CAS  PubMed  Google Scholar 

  62. Wickler, W. in Primate Ethology (ed. Morris, D.) 69–147 (Wiedenfeld and Nicolson, 1967).

  63. Vasey, P. L. Same-sex sexual partner preference in hormonally and neurologically unmanipulated animals. Ann. Rev. Sex. Res. 13, 141–179 (2002).

    Google Scholar 

  64. Tomasello, M. & Call, J. Primate Cognition (Oxford Univ. Press, 1997).

  65. Paciulli, L. M. & Emer, L. K. in The International Encyclopedia of Biological Anthropology (eds Trevathan, W. et al.) 1–2 (Wiley, 2018).

  66. Manson, J. H. Male dominance and mount series duration in Cayo Santiago rhesus macaques. Anim. Behav. 51, 1219–1231 (1996).

    Article  Google Scholar 

  67. Dubuc, C., Allen, W. L., Maestripieri, D. & Higham, J. P. Is male rhesus macaque red color ornamentation attractive to females? Behav. Ecol. Sociobiol. 68, 1215–1224 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Widdig, A. et al. Low incidence of inbreeding in a long-lived primate population isolated for 75 years. Behav. Ecol. Sociobiol. 71, 18 (2017).

    Article  PubMed  Google Scholar 

  69. Balasubramaniam, K. N., Dunayer, E. S., Gilhooly, L. J., Rosenfield, K. A. & Berman, C. M. Group size, contest competition and social structure in Cayo Santiago rhesus macaques. Behaviour 151, 1759–1798 (2014).

    Article  Google Scholar 

  70. Kumar, R., Sinha, A. & Radhakrishna, S. Comparative demography of two commensal macaques in India: implications for population status and conservation. Folia Primatol. 84, 384–393 (2013).

    Article  Google Scholar 

  71. Southwick, C. H., Beg, M. A. & Siddiqi, M. R. A population survey of rhesus monkeys in villages, towns and temples of northern India. Ecology 42, 538–547 (1961).

    Article  Google Scholar 

  72. Widdig, A. et al. Genetic studies on the Cayo Santiago rhesus macaques: a review of 40 years of research. Am. J. Primatol. 78, 44–62 (2016).

    Article  PubMed  Google Scholar 

  73. Lee, D. S., Mandalaywala, T. M., Dubuc, C., Widdig, A. & Higham, J. P. Higher early life mortality with lower infant body mass in a free‐ranging primate. J. Anim. Ecol. 89, 2300–2310 (2020).

    Article  PubMed  Google Scholar 

  74. Blomquist, G. E. Maternal effects on offspring mortality in rhesus macaques (Macaca mulatta). Am. J. Primatol. 75, 238–251 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  75. Melnick, D. J., Pearl, M. C. & Richard, A. F. Male migration and inbreeding avoidance in wild rhesus monkeys. Am. J. Primatol. 7, 229–243 (1984).

    Article  PubMed  Google Scholar 

  76. Gamer, M., Lemon, J., Fellows, I. & Singh, P. irr: Various Coefficients of Interrater Reliability and Agreement. R Package v.0.84.1 (Cran, 2012).

  77. Hadfield, J. D. MCMCglmm: MCMC methods for multi-response GLMMs in R. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  78. David, H. A. Ranking from unbalanced paired-comparison data. Biometrika 74, 432–436 (1987).

    Article  Google Scholar 

  79. Neumann, C. et al. Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim. Behav. 82, 911–921 (2011).

    Article  Google Scholar 

  80. Balasubramaniam, K. N. et al. Consistency of dominance rank order: a comparison of David’s scores with I&SI and Bayesian methods in macaques. Am. J. Primatol. 75, 959–971 (2013).

    Article  CAS  PubMed  Google Scholar 

  81. Dubuc, C. et al. Sexually selected skin colour is heritable and related to fecundity in a non-human primate. Proc. R. Soc. B. 281, 20141602 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Kimock, C. M., Dubuc, C., Brent, L. J. & Higham, J. P. Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate. Sci. Rep. 9, 19794 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Wilson, A. J. How should we interpret estimates of individual repeatability? Evol. Lett. 2, 4–8 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Roche, D. G., Careau, V. & Binning, S. A. Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists. J. Exp. Biol. 219, 3832–3843 (2016).

    PubMed  Google Scholar 

  85. Dochtermann, N. A., Schwab, T. & Sih, A. The contribution of additive genetic variation to personality variation: heritability of personality. Proc. R. Soc. B. 282, 20142201 (2014).

    Article  Google Scholar 

  86. Wolak, M. E. Nadiv: an R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Meth. Ecol. Evol. 3, 792–796 (2012).

    Article  Google Scholar 

  87. Kruuk, L. E. B., Slate, J. & Wilson, A. J. New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Ann. Rev. Ecol. Evol. Syst. 39, 525–548 (2008).

    Article  Google Scholar 

  88. Reynolds, C. A. Behavioral Genetics 6th edn (Springer, 2013).

  89. Dochtermann, N. A., Schwab, T., Berdal, M. A., Dalos, J. & Royauté, R. The heritability of behavior: a meta-analysis. J. Hered. 110, 403–410 (2019).

    Article  PubMed  Google Scholar 

  90. Mousseau, T. A. & Roff, D. A. Natural selection and the heritability of fitness components. Heredity 59, 181–197 (1987).

    Article  PubMed  Google Scholar 

  91. Kruuk, L. E. B. et al. Heritability of fitness in a wild mammal population. Proc. Natl Acad. Sci. USA 97, 698–703 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Bonnet, T. et al. Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals. Science 376, 1012–1016 (2022).

    Article  CAS  PubMed  Google Scholar 

  93. Wolak, M. E. & Reid, J. M. Accounting for genetic differences among unknown parents in microevolutionary studies: how to include genetic groups in quantitative genetic animal models. J. Anim. Ecol. 86, 7–20 (2017).

    Article  PubMed  Google Scholar 

  94. Nakagawa, S. & Schielzeth, H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935–956 (2010).

    PubMed  Google Scholar 

  95. Nakagawa, S., Johnson, P. C. D. & Schielzeth, H. The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J. R. Soc. Int. 14, 20170213 (2017).

    Article  Google Scholar 

  96. de Villemereuil, P., Schielzeth, H., Nakagawa, S. & Morrissey, M. General methods for evolutionary quantitative genetic inference from generalized mixed models. Genetics 204, 1281–1294 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  97. de Villemereuil, P., Morrissey, M. B., Nakagawa, S. & Schielzeth, H. Fixed‐effect variance and the estimation of repeatabilities and heritabilities: issues and solutions. J. Evol. Biol. 31, 621–632 (2018).

    Article  PubMed  Google Scholar 

  98. Kasper, C., Kölliker, M., Postma, E. & Taborsky, B. Consistent cooperation in a cichlid fish is caused by maternal and developmental effects rather than heritable genetic variation. Proc. R. Soc. B. 284, 20170369 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Araya‐Ajoy, Y. G. & Dingemanse, N. J. Repeatability, heritability and age‐dependence of seasonal plasticity in aggressiveness in a wild passerine bird. J. Anim. Ecol. 86, 227–238 (2017).

    Article  PubMed  Google Scholar 

  100. Amadeu, R. R. et al. AGHmatrix: R package to construct relationship matrices for autotetraploid and diploid species: a blueberry example. Plant Genome 9, plantgenome2016-01 (2016).

    Article  Google Scholar 

  101. Kulik, L., Muniz, L., Mundry, R. & Widdig, A. Patterns of interventions and the effect of coalitions and sociality on male fitness. Mol. Ecol. 21, 699–714 (2012).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  103. Furuichi, T. Social interactions and the life history of female Pan paniscus in Wamba, Zaire. Int. J. Primatol. 10, 173–197 (1989).

    Article  Google Scholar 

  104. Idani, G. I. Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol. 57, 83–95 (1991).

    Article  CAS  Google Scholar 

  105. Fairbanks, L. A., McGuire, M. T. & Kerber, W. Sex and aggression during rhesus monkey group formation. Aggress. Behav. 3, 241–249 (1977).

    Article  Google Scholar 

  106. Mitchell, C. L. Migration alliances and coalitions among adult male South American squirrel monkeys (Saimiri sciureus). Behaviour 130, 169–190 (1994).

    Article  Google Scholar 

  107. Houslay, T. M., Nielsen, J. F. & Clutton‐Brock, T. H. Contributions of genetic and nongenetic sources to variation in cooperative behavior in a cooperative mammal. Evolution 75, 3071–3086 (2021).

    Article  PubMed  Google Scholar 

  108. Godoy, I., Korsten, P. & Perry, S. E. Genetic, maternal and environmental influences on sociality in a pedigreed primate population. Heredity 129, 203–214 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Lange, E. C. et al. Heritable and sex-specific variation in the development of social behavior in a wild primate. Preprint at bioRxiv https://doi.org/10.1101/2022.10.21.513189 (2022).

  110. Nichols, H. J. et al. A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses. Ecol. Lett. 24, 1966–1975 (2021).

    Article  PubMed  Google Scholar 

  111. McLean, E. R., Moorad, J., Tung, J., Archie, E. A. & Alberts, S. C. Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate. Evolution https://doi.org/10.1093/evolut/qpad066 (2023).

  112. Långström, N., Rahman, Q., Carlström, E. & Lichtenstein, P. Genetic and environmental effects on same-sex sexual behavior: a population study of twins in Sweden. Arch. Sex. Behav. 39, 75–80 (2010).

    Article  PubMed  Google Scholar 

  113. Kirk, K. M., Bailey, J. M., Dunne, M. P. & Martin, N. G. Measurement models for sexual orientation in a community twin sample. Behav. Genet. 30, 345–356 (2000).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank S. Edwards, S. Radonich, D. Phillips, J. Negrón, G. Caraballo, N. Rivera, B. Giura, E. Maldonado, J. Resto, A. R. Lambides, A. Arre and other staff at the Caribbean Primate Research Centre for support and advice during fieldwork and data collection; J. Higham, A. Leroi and R. Holt. We thank the UK Natural Environment Research Council (grant numbers: NE/S007415/1, NE/R012229/1; J.C., E.F. and V.S.), the American Institute of Bisexuality (J.C. and V.S.), the Genetics Society (J.C.) and the Evolution Education Trust (V.S.) for funding. The Cayo Santiago monkey population is currently supported by the University of Puerto Rico (UPR) and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (grant number 2P40OD012217). The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of the UPR or ORIP. Finally, for the purpose of open access, the corresponding author has applied a ‘Creative Commons Attribution’ (CC BY) licence to any author-accepted manuscript version arising from this work.

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  1. Georgina Mace Centre for the Living Planet, Department of Life Sciences, Silwood Park Campus, Imperial College London, Ascot, UK

    Jackson Clive, Ewan Flintham & Vincent Savolainen

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J.C. collected behavioural data, designed and performed analyses, and wrote the initial manuscript, with subsequent drafting from V.S., E.F. and J.C.; V.S. conceived and supervised the research.

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Correspondence to Vincent Savolainen.

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Clive, J., Flintham, E. & Savolainen, V. Same-sex sociosexual behaviour is widespread and heritable in male rhesus macaques. Nat Ecol Evol 7, 1287–1301 (2023). https://doi.org/10.1038/s41559-023-02111-y

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