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Social and sexual behaviors predict immune system activation, but not adrenocortical activation, in male rhesus macaques

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Abstract

Social interactions are well known to influence fitness in social animals, but the physiological processes that connect the two remain largely unknown. This study aimed to explore how variation in sociality influences the adrenocortical and/or immune system in the rhesus macaque, a seasonally breeding species engaging in indirect male-male mating competition. We collected data on 18 adult male rhesus macaques living on Cayo Santiago over 4 months during the mating season. We assessed fecal glucocorticoids (fGCs), a marker of the physiological stress response, and urinary neopterin (uNEO), a marker of immune system activation. We predicted that males who spent more time affiliated with groupmates would have decreased fGCs due to the physiological buffering potential of positive social interaction and increased uNEO associated with increased exposure to disease. Additionally, we predicted that uNEO would increase in response to copulation, consortship, and as the mating season progressed due to infection associated with sexual behavior. Although none of our sociosexual behaviors of interest predicted fGCs, the proportion of time males spent grooming, and specifically the proportion of time males spent receiving grooming from juveniles, was positively associated with concurrent uNEO concentrations. Copulation was negatively correlated with concurrent uNEO, and uNEO, but not fGCs, increased as the mating season progressed. These results indicate that certain social behaviors are associated with immune system activation and provide a putative physiological link between the physical demands of endurance rivalry and mortality commonly observed in males of this species.

Significance statement

Social interactions can strongly influence health in social animals, possibly mediated through the endocrine and/or immune system. We investigated how affiliative social and sexual interactions influence these systems in male rhesus macaques by non-invasively measuring hormones associated with energy allocation and responses to stressors (glucocorticoids) and a marker of immune system activation (neopterin). The sociosexual behaviors measured here did not appear to covary with glucocorticoid concentrations; however, higher neopterin concentrations were observed when males spent more time grooming. We also found that males spent less time copulating when their neopterin concentrations were high and that there is a general increase in neopterin concentrations as the mating season progresses. Our results show that variation in social and sexual behavior is associated with neopterin production in the rhesus macaque, suggesting that social investment by groupmates and disease transmission may be important factors mediating the relationship between sociality and fitness in social species.

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Data availability

All data and code are currently publicly available on Open Science Framework at https://doi.org/10.17605/OSF.IO/E3MD5.

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Acknowledgements

We thank Louisa Radosevich and Connie Rojas for their help with data collection and Allegra DePasquale and Andrea Heistermann for their help with the laboratory analyses. RMP thanks Megan Petersdorf and Alex DeCasien for feedback during the project. We thank two anonymous reviewers for constructive comments which improved the manuscript.

Funding

This work was funded by an intramural grant from NYU to JPH from the University Research Challenge Fund (URCF).

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Authors and Affiliations

  1. Department of Anthropology, New York University, 25 Waverly Place, New York, NY, 10003, USA

    Rachel M. Petersen & James P. Higham

  2. Endocrinology Laboratory, German Primate Center, Kellnerweg 4, D-37077, Göttingen, Germany

    Michael Heistermann

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  1. Rachel M. Petersen
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  3. James P. Higham
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Contributions

Study conception, design, and funding were provided by JPH, glucocorticoid analyses were performed by MH, and neopterin and data analyses were performed by JPH and RMP. The first draft of the manuscript was written by RMP, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Rachel M. Petersen.

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Ethical approval

The New York University and University of Puerto Rico IACUC approved of this study protocol (NYU protocol #14-1439, UPR #A150116). All applicable national and institutional guidelines for the use of animals were followed. All study methods were non-invasive, and observers maintained a distance of 5 m from study subjects.

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The authors declare no competing interests.

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Communicated by B. Voelkl

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Petersen, R.M., Heistermann, M. & Higham, J.P. Social and sexual behaviors predict immune system activation, but not adrenocortical activation, in male rhesus macaques. Behav Ecol Sociobiol 75, 159 (2021). https://doi.org/10.1007/s00265-021-03083-4

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