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An agent-based model of the female rivalry hypothesis for concealed ovulation in humans

Nature Human Behaviour volume 5, pages 726–735 (2021)Cite this article

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Abstract

After half a century of debate and few empirical tests, there remains no consensus concerning why ovulation in human females is considered concealed. The predominant male investment hypothesis states that females were better able to obtain material investment from male partners across those females’ ovulatory cycles by concealing ovulation. We build on recent work on female competition to propose and investigate an alternative—the female rivalry hypothesis—that concealed ovulation benefited females by allowing them to avoid aggression from other females. Using an agent-based model of mating behaviour and paternal investment in a human ancestral environment, we did not find strong support for the male investment hypothesis, but found support for the female rivalry hypothesis. Our results suggest that concealed ovulation may have benefitted females in navigating their intrasexual social relationships. More generally, this work implies that explicitly considering female–female interactions may inspire additional insights into female behaviour and physiology.

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Fig. 1: Flowchart summarizing the schedule for our agent-based model for both female and male agents.
Fig. 2: Lifetime reproductive success of revealers and concealers after 10,000 time steps in the model.
Fig. 3: Effects of varying the percentage of promiscuous males in the population.

Data availability

This study was pre-registered on the OSF. Open data and analysis code can be found in our OSF repository at https://osf.io/c5pq7/.

Code availability

NetLogo models can be found in our OSF repository at https://osf.io/c5pq7/.

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Acknowledgements

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Authors and Affiliations

  1. The Oklahoma Center for Evolutionary Analysis (OCEAN), Department of Psychology, Oklahoma State University, Stillwater, OK, USA

    Jaimie Arona Krems

  2. School of Psychology, University of Auckland, Auckland, New Zealand

    Scott Claessens

  3. Department of Psychology, Arizona State University, Tempe, AZ, USA

    Scott Claessens, Marco Campenni & Athena Aktipis

  4. Interdisciplinary Cooperation Initiative, Arizona State University, Tempe, AZ, USA

    Scott Claessens, Marco Campenni & Athena Aktipis

  5. Department of Psychology, University of California, Los Angeles, CA, USA

    Melissa R. Fales & Martie G. Haselton

  6. Center for Behavior, Evolution, and Culture, University of California, Los Angeles, CA, USA

    Melissa R. Fales & Martie G. Haselton

  7. Centre for Ecology and Conservation, University of Exeter, Exeter, UK

    Marco Campenni

  8. Department of Communication, University of California, Los Angeles, CA, USA

    Martie G. Haselton

  9. Institute for Society and Genetics, University of California, Los Angeles, CA, USA

    Martie G. Haselton

  10. Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA

    Athena Aktipis

  11. Arizona Cancer Evolution Center, Arizona State University, Tempe, AZ, USA

    Athena Aktipis

  12. Biodesign Center for Biocomputation, Security and Society, Arizona State University, Tempe, AZ, USA

    Athena Aktipis

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Contributions

J.A.K., S.C., M.G.H. and A.A. developed and/or critically enhanced the underlying theorizing. J.A.K., M.R.F., M.C. and A.A. researched the underlying model parameters. A.A. wrote the initial model, which was subsequently modified by S.C. and M.C. S.C. and A.A. ran and reported the analyses. S.C. created all of the figures. J.A.K., S.C. and A.A. wrote and revised the manuscript with critical feedback from M.G.H. All authors approved the manuscript.

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Correspondence to Athena Aktipis.

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Extended data

Extended Data Fig. 1 The paternal investment for Revealers and Concealers, after 10,000 time steps in the model.

Violin plots summarise the results of 10,000 independent model runs, bolded points are mean averages, and error bars are standard errors. Concealers consistently outcompete Revealers only in Experiment 3, under conditions of female aggression towards ovulating rivals. See Supplementary Table 5 for inferential statistics.

Extended Data Fig. 2 Varying the female attractiveness multiplier when fertile.

For both (a) reproductive success and (b) paternal investment, Concealers have an advantage over Revealers regardless of the fertility multiplier for Revealers. Points are mean averages across 100 independent model runs per parameter value, and error bars are standard errors. See Supplementary Table 6 for inferential statistics.

Extended Data Fig. 3 Varying the radius of competition (females) and mate search (males).

For both (a) reproductive success and (b) paternal investment, Concealers have an advantage over Revealers regardless of the radius of competition or mate search. Points are mean averages across 100 independent model runs per parameter value, and error bars are standard errors. See Supplementary Table 6 for inferential statistics.

Extended Data Fig. 4 Further sensitivity analyses.

We vary the offspring investment amount (units) required to successful have a child in the model, the number of individuals in the model (population size), the proportion of females in the population, the proportion of Concealers within the female population, and the size of the square world (lattice width is equal to lattice height). In all cases, Concealers have an advantage over Revealers. Points are mean averages across 100 independent model runs per parameter value, and error bars are standard errors. See Supplementary Table 6 for inferential statistics.

Extended Data Fig. 5 Varying the decay of aggression damage (that is, the speed at which females heal from aggression), where 0 means females never heal, and 1 means females heal immediately.

For both (a) reproductive success and (b) paternal investment, Concealers only have an advantage when the decay of aggression damage is less than or equal to around 0.6. Points are mean averages across 100 independent model runs per parameter value, and error bars are standard errors. See Supplementary Table 6 for inferential statistics.

Extended Data Fig. 6 Tile plots summarizing the Concealer advantage with varying costs of aggression, to both self and other (target).

As tiles become increasingly beige, Concealers have more of an advantage (that is, positive raw difference in either number of children or paternal investment units). For both (a) reproductive success and (b) paternal investment, Concealers only have an advantage when the cost to self is low (< 1), and the cost to other is positive (> 0). Values are averaged over 100 independent model runs per parameter value. See Supplementary Table 6 for inferential statistics.

Extended Data Fig. 7 The number of aggression acts Concealers and Revealers received after 10,000 time steps in the model, across 20 different model runs all with the default parameters for Experiment 2, where females aggressed towards the most attractive female nearby females (not necessarily the ovulating females).

Concealers received 294 acts of aggression on average (SD = 131). Revealers received 308 acts of aggression on average (SD = 127), significantly more than Concealers (GLMM; p = 0.01). Aggression amounts appear normally distributed, with few outliers.

Extended Data Fig. 8 The number of aggression acts each Revealer received after 10,000 time steps in the model, across 20 different model runs all with the default parameters for Experiment 3, where females aggressed towards the nearby ovulating females.

Concealers were never the targets of aggression. Revealers received 941 acts of aggression on average (SD = 312). Aggression amounts appear normally distributed, with few outliers.

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Supplementary Results, ODD protocol, and Supplementary Tables 1–4.

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Krems, J.A., Claessens, S., Fales, M.R. et al. An agent-based model of the female rivalry hypothesis for concealed ovulation in humans. Nat Hum Behav 5, 726–735 (2021). https://doi.org/10.1038/s41562-020-01038-9

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