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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.

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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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