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Mating Competition, Promiscuity, and Life History Traits as Predictors of Sexually Transmitted Disease Risk in Primates

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Abstract

Competition among males influences the distribution of copulations and should therefore influence the spread of sexually transmitted diseases (STDs). We developed a model to investigate STDs in the mating and social systems found in primates, and we tested predictions using comparative methods. In the model, groups were distributed on a square lattice in which males or females disperse and males undergo characteristic dominance trajectories at maturity (challenge vs. queuing). We investigated the impact of mating rate, mating skew, migration rate of males or females, and group size on disease spread and prevalence. The model generated several predictions: 1) STD prevalence is higher in females than males; 2) STD risk increases with copulation rate; 3) high skew is negatively associated with STD risk; 4) STD risk is higher for all individuals when females disperse and 5) when mortality rates are lower; and 6) reproductive skew and later age of male dominance (queuing) produce more strongly female-biased STD prevalence. In comparative tests, we quantified STD risk as prevalence and richness of sexually transmitted organisms at the host species level. We found positive associations between host longevity and higher STD richness, and only (nonsignificant) weak trends for females to have higher STD prevalence. Mating skew showed a weakly positive association with STD richness, contrary to predictions of our model but consistent with predictions from a previous model. In some tests, we also found that female dispersal resulted in greater STD infection risk. Collectively, these results demonstrate that mating competition and demography influence patterns of STD infection, with mortality rates having the strongest effects in comparative tests.

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Acknowledgments

We especially thank Randi Griffin for coding the model and providing extensive feedback on the design, implementation, and interpretation of the findings. We thank two reviewers and the editors of this special issue for their feedback. Joel Bray helped compile data used for the comparative tests and provided feedback on the text. For funding, N. Kutsukake thanks PRESTO (JST) and Kakenhi (25711025, MEXT), and E. J. Scully acknowledges support from an National Science Foundation Graduate Research Fellowship.

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Authors and Affiliations

  1. Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, 02138, USA

    Charles L. Nunn & Erik J. Scully

  2. Department of Evolutionary Anthropology, Duke University, Durham, North Carolina, 27708, USA

    Charles L. Nunn

  3. Duke Global Health Institute, Durham, North Carolina, 27710, USA

    Charles L. Nunn

  4. Department of Evolutionary Studies of Biosystems, The Graduate University for Advanced Studies, Hayama-cho, Kanagawa, 240-0193, Japan

    Nobuyuki Kutsukake

  5. PRESTO Researcher, Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama, Japan

    Nobuyuki Kutsukake

  6. Courant Research Centre Evolution of Social Behaviour, Georg-August University Göttingen, 37077, Göttingen, Germany

    Julia Ostner & Oliver Schülke

  7. CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia

    Peter H. Thrall

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  1. Charles L. Nunn
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  2. Erik J. Scully
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  3. Nobuyuki Kutsukake
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  4. Julia Ostner
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  5. Oliver Schülke
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Correspondence to Charles L. Nunn.

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Fig. S1

Effects of sex-biased dispersal and female group size (n f ) on (a) population prevalence and (b) sex differences in prevalence (calculated as female prevalence minus male prevalence). Filled circles indicate male dispersal. Open circles indicate female dispersal. (PPTX 223 kb)

Fig. S2

Effects of sex-biased dispersal and peak age of dominance (p) on (a) population prevalence and (b) sex differences in prevalence (calculated as female prevalence minus male prevalence). Filled circles indicate male dispersal. Open circles indicate female dispersal. (PPTX 225 kb)

Fig. S3

Effects of sex-biased dispersal and migration rate (m r ) on (a) population prevalence and (b) sex differences in prevalence (calculated as female prevalence minus male prevalence). Filled circles indicate male dispersal. Open circles indicate female dispersal. (PPTX 214 kb)

Fig. S4

Effects of sex-biased dispersal and migration rate (c r ) on (a) population prevalence and (b) sex differences in prevalence (calculated as female prevalence minus male prevalence). Filled circles indicate male dispersal. Open circles indicate female dispersal. (PPTX 222 kb)

Fig. S5

Effects of sex-biased dispersal and mortality rate (d) on (a) population prevalence and (b) sex differences in prevalence (calculated as female prevalence minus male prevalence). Filled circles indicate male dispersal. Open circles indicate female dispersal. (PPTX 216 kb)

IJOP_D-13-00138R2_ESM_Main_data.xlsx (XLSX 21 kb)

IJOP-D-13-00138R2_ESM_TreeBlock_10kTrees_Primates_Version3.nex-1.txt (TXT 74 kb)

IJOP-D-13-00138R2_ESM_STD_Model_Code.R (R 8 kb)

IJOP-D-13-00138R2_ESM_Eq_Prev.docx (DOCX 1307 kb)

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Nunn, C.L., Scully, E.J., Kutsukake, N. et al. Mating Competition, Promiscuity, and Life History Traits as Predictors of Sexually Transmitted Disease Risk in Primates. Int J Primatol 35, 764–786 (2014). https://doi.org/10.1007/s10764-014-9781-5

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