Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

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/.

References

  1. Dixson, A. F. in Advances in the Study of Behavior Vol. 13 (eds Rosenblatt, J. S. et al.) 63–106 (Academic Press, 1983).

  2. Deschner, T., Heistermann, M., Hodges, K. & Boesch, C. Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm. Behav. 46, 204–215 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Nunn, C. L. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58, 229–246 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Alexander, R. D. & Noonan, K. M. Concealment of ovulation, parental care, and human social evolution. in Evolutionary Biology and Human Social Behavior: An Anthropological Perspective (eds. Chagnon, N. & Irons, W.) 436–453 (Duxbury Press, 1979).

  5. Benshoof, L. & Thornhill, R. The evolution of monogamy and concealed ovulation in humans. J. Soc. Biol. Struct. 2, 95–106 (1979).

    Article  Google Scholar 

  6. Burley, N. The evolution of concealed ovulation. Am. Nat. 114, 835–858 (1979).

    Article  Google Scholar 

  7. Burt, A. ‘Concealed ovulation’ and sexual signals in primates. Folia Primatol. 58, 1–6 (1992).

    Article  CAS  Google Scholar 

  8. Etkin, W. Social behavioral factors in the emergence of man. Hum. Biol. 35, 299–310 (1963).

    CAS  PubMed  Google Scholar 

  9. Hill, K. Hunting and human evolution. J. Hum. Evol. 11, 521–544 (1982).

    Article  Google Scholar 

  10. Hrdy, S. B. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 13–40 (1979).

    Article  Google Scholar 

  11. Kourtovik, D. Hominization and the loss of the oestrus. J. Hum. Evol. 12, 696 (1983).

    Article  Google Scholar 

  12. Lovejoy, C. O. The origin of man. Science 211, 341–350 (1981).

    Article  CAS  PubMed  Google Scholar 

  13. Miller, E. M. Concealed ovulation as a strategy for increasing per capita paternal investment. Mank. Q. 36, 297–334 (1996).

    Article  Google Scholar 

  14. Pawłowski, B. Loss of oestrus and concealed ovulation in human evolution: the case against the sexual-selection hypothesis. Curr. Anthropol. 40, 257–276 (1999).

    Article  Google Scholar 

  15. Schoröder, I. Concealed ovulation and clandestine copulation: a female contribution to human evolution. Ethol. Sociobiol. 14, 381–389 (1993).

    Article  Google Scholar 

  16. Spuhler, J. N. Continuities and discontinuities in anthropoid-hominid behavioral evolution: bipedal locomotion and sexual receptivity. in Evolutionary Biology and Human Social Behavior: An Anthropological Perspective (eds. Chagnon, N. & Irons, W.) 454–461 (Duxbury Press, 1979).

  17. Strassmann, B. I. Sexual selection, paternal care, and concealed ovulation in humans. Evol. Hum. Behav. 2, 31–40 (1981).

    Google Scholar 

  18. Symons, D. The Evolution of Human Sexuality (Oxford Univ. Press, 1979).

  19. Turke, P. W. Effects of ovulatory concealment and synchrony on protohominid mating systems and parental roles. Evol. Hum. Behav. 5, 33–44 (1984).

    Google Scholar 

  20. Turke, P. W. Concealed ovulation, menstrual synchrony and paternal investment. in Biosocial Perspectives on the Family (ed. Filsinger, E. E.) 119–136 (Sage Publications, 1988).

  21. Björkqvist, K., Lagerspetz, K. M. J. & Kaukiainen, A. Do girls manipulate and boys fight? Developmental trends in regard to direct and indirect aggression. Aggress. Behav. 18, 117–127 (1992).

    Article  Google Scholar 

  22. Campbell, A. A few good men: evolutionary psychology and female adolescent aggression. Ethol. Sociobiol. 16, 99–123 (1995).

    Article  Google Scholar 

  23. Campbell, A. A Mind Of Her Own: The Evolutionary Psychology of Women (Oxford Univ. Press, 2013).

  24. Fisher, M. L. Female intrasexual competition decreases female facial attractiveness. Proc. Biol. Sci. 271, S283–S285 (2004).

    Article  PubMed Central  Google Scholar 

  25. Lagerspetz, K. M. J., Björkqvist, K. & Peltonen, T. Is indirect aggression typical of females? Gender differences in aggressiveness in 11-to 12-year-old children. Aggress. Behav. 14, 403–414 (1988).

    Article  Google Scholar 

  26. McAndrew, F. T. The ‘sword of a woman’: gossip and female aggression. Aggress. Violent Behav. 19, 196–199 (2014).

    Article  Google Scholar 

  27. Rucas, S. L. et al. Female intrasexual competition and reputational effects on attractiveness among the Tsimane of Bolivia. Evol. Hum. Behav. 27, 40–52 (2006).

    Article  Google Scholar 

  28. Vaillancourt, T. Do human females use indirect aggression as an intrasexual competition strategy. Phil. Trans. R. Soc. Lond. B Biol. Sci. 368, 20130080 (2013).

    Article  Google Scholar 

  29. Crick, N. R. & Grotpeter, J. K. Relational aggression, gender, and social-psychological adjustment. Child Dev. 66, 710–722 (1995).

    Article  CAS  PubMed  Google Scholar 

  30. Benenson, J. F. Warriors and Worriers: The Survival of the Sexes (Oxford Univ. Press, 2014).

  31. Hrdy, S. B. “Nepotists” and “altruists”: the behavior of old females among macaques and langur monkeys. in Other Ways of Growing Old: Anthropological Perspectives (eds. Amoss, P. T. & Harrell, S.) 59–76 (Stanford Univ. Press, 1981).

  32. Campbell, A. Female competition: causes, constraints, content, and contexts. J. Sex Res. 41, 16–26 (2004).

    Article  PubMed  Google Scholar 

  33. Gangestad, S. W. & Thornhill, R. Human oestrus. Proc. Biol. Sci. 275, 991–1000 (2008).

    PubMed  PubMed Central  Google Scholar 

  34. Thornhill, R. & Gangestad, S. W. The Evolutionary Biology of Human Female Sexuality (Oxford Univ. Press, 2008).

  35. Wolfe, L. D. Human evolution and the sexual behavior of female primates. in Understanding Behavior: What Primate Studies Tell Us about Human Behavior (eds. Loy, J. D. & Peters, C. B.) 121–151 (Oxford Univ. Press, 1991).

  36. Sillen-Tullberg, B. & Moller, A. P. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Am. Nat. 141, 1–25 (1993).

    Article  CAS  PubMed  Google Scholar 

  37. Lobmaier, J. S., Bobst, C. & Probst, F. Can women detect cues to ovulation in other women’s faces? Biol. Lett. 12, 20150638 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Haselton, M. G. & Gildersleeve, K. Can men detect ovulation? Curr. Dir. Psychol. Sci. 20, 87–92 (2011).

    Article  Google Scholar 

  39. Bryant, G. A. & Haselton, M. G. Vocal cues of ovulation in human females. Biol. Lett. 5, 12–15 (2009).

    Article  PubMed  Google Scholar 

  40. Thornhill, R. et al. MHC, symmetry and body scent attractiveness in men and women (Homo sapiens). Behav. Ecol. 14, 668–678 (2003).

    Article  Google Scholar 

  41. Pipitone, R. N. & Gallup, G. G. Women’s voice attractiveness varies across the menstrual cycle. Evol. Hum. Behav. 29, 268–274 (2008).

    Article  Google Scholar 

  42. Bobst, C. & Lobmaier, J. S. Men’s preference for the ovulating female is triggered by subtle face shape differences. Horm. Behav. 62, 413–417 (2012).

    Article  PubMed  Google Scholar 

  43. Hurtado, A. M. & Hill, K. R. Paternal effect on offspring Survivorship among Ache and Hiwi hunter-gatherers: implications for modeling pair-bond stability. in Father–Child Relations Cultural and Biosocial Contexts (ed. Hewlett, B. S.) 31–55 (Routledge, 1992).

  44. Grebe, N. M., Gangestad, S. W., Garver-Apgar, C. E. & Thornhill, R. Women’s luteal-phase sexual proceptivity and the functions of extended sexuality. Psychol. Sci. 24, 2106–2110 (2013).

    Article  PubMed  Google Scholar 

  45. Clutton-Brock, T. Sexual selection in females. Anim. Behav. 77, 3–11 (2009).

    Article  Google Scholar 

  46. Benenson, J. F. The development of human female competition: allies and adversaries. Phil. Trans. R. Soc. Lond. B Biol. Sci. 368, 20130079 (2013).

    Article  Google Scholar 

  47. Campbell, A. Staying alive: evolution, culture, and women’s intrasexual aggression. Behav. Brain Sci. 22, 203–214 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Liesen, L. T. in Evolution’s Empress: Darwinian Perspectives on the Nature of Women (eds Fisher, M. L. et al.) 43–62 (Oxford Univ. Press, 2013).

  49. Liesen, L. T. Feminist and evolutionary perspectives of female-female competition, status seeking, and social network formation. in Handbook of Women and Competition (ed. Fisher, M. L.) 71–87 (Oxford Univ. Press, 2018).

  50. Archer, J. Sex differences in aggression in real-world settings: a meta-analytic review. Rev. Gen. Psychol. 8, 291–322 (2004).

    Article  Google Scholar 

  51. Björkqvist, K. Sex differences in physical, verbal, and indirect aggression: a review of recent research. Sex Roles 30, 177–188 (1994).

    Article  Google Scholar 

  52. Burbank, V. K. Female aggression in cross-cultural perspective. Behav. Sci. Res. 21, 70–100 (1987).

    Article  Google Scholar 

  53. Hess, N. H. & Hagen, E. H. Sex differences in indirect aggression: psychological evidence from young adults. Evol. Hum. Behav. 27, 231–245 (2006).

    Article  Google Scholar 

  54. Huchard, E. & Cowlishaw, G. Female–female aggression around mating: an extra cost of sociality in a multimale primate society. Behav. Ecol. 22, 1003–1011 (2011).

    Article  Google Scholar 

  55. Stockley, P. & Bro-Jørgensen, J. Female competition and its evolutionary consequences in mammals. Biol. Rev. Camb. Phil. Soc. 86, 341–366 (2011).

    Article  Google Scholar 

  56. Harding, R. M. et al. Evidence for variable selective pressures at MC1R. Am. J. Hum. Genet. 66, 1351–1361 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Cacioppo, S. & Hatfield, E. Passionate love and sexual desire. in The International Encyclopedia of Human Sexuality Vol. 7 (eds Bolin, A. & Whelehan, P.) 861–1042 (Wiley, 2015).

  58. De Vleeschouwer, K., Van Elsacker, L. & Leus, K. Multiple breeding females in captive groups of golden-headed lion tamarins (Leontopithecus chrysomelas): causes and consequences. Folia Primatol. 72, 1–10 (2001).

    Article  CAS  Google Scholar 

  59. Wasser, S. K. & Starling, A. K. Proximate and ultimate causes of reproductive suppression among female yellow baboons at Mikumi National Park, Tanzania. Am. J. Primatol. 16, 97–121 (1988).

    Article  PubMed  Google Scholar 

  60. Krems, J. A., Neuberg, S. L., Filip-Crawford, G. & Kenrick, D. T. Is she angry? (Sexually desirable) women “see” anger on female faces. Psychol. Sci. 26, 1655–1663 (2015).

    Article  PubMed  Google Scholar 

  61. Fisher, M. & Cox, A. The influence of female attractiveness on competitor derogation. J. Evol. Psychol. 7, 141–155 (2009).

    Article  Google Scholar 

  62. Campbell, A. & Muncer, S. Sex differences in aggression: social representation and social roles. Br. J. Soc. Psychol. 33, 233–240 (1994).

    Article  PubMed  Google Scholar 

  63. Hurst, A. C., Alquist, J. L. & Puts, D. A. Women’s fertility status alters other women’s jealousy and mate guarding. Pers. Soc. Psychol. Bull. 43, 191–203 (2017).

    Article  PubMed  Google Scholar 

  64. Krems, J. A., Neel, R., Neuberg, S. L., Puts, D. A. & Kenrick, D. T. Women selectively guard their (desirable) mates from ovulating women. J. Pers. Soc. Psychol. 110, 551–573 (2016).

    Article  PubMed  Google Scholar 

  65. Krems, J. A., Rankin, A. M. & Northover, S. B. Women’s strategic defenses against same-sex aggression: evidence from sartorial behavior. Soc. Psychol. Personal. Sci. 11, 770–781 (2020).

    Article  Google Scholar 

  66. Leenaars, L. S., Dane, A. V. & Marini, Z. A. Evolutionary perspective on indirect victimization in adolescence: the role of attractiveness, dating and sexual behavior. Aggress. Behav. 34, 404–415 (2008).

    Article  PubMed  Google Scholar 

  67. Vaillancourt, T. & Sharma, A. Intolerance of sexy peers: intrasexual competition among women. Aggress. Behav. 37, 569–577 (2011).

    Article  PubMed  Google Scholar 

  68. Elliot, A. J., Greitemeyer, T. & Pazda, A. D. Women’s use of red clothing as a sexual signal in intersexual interaction. J. Exp. Soc. Psychol. 49, 599–602 (2013).

    Article  Google Scholar 

  69. Pazda, A. D., Prokop, P. & Elliot, A. J. Red and romantic rivalry: viewing another woman in red increases perceptions of sexual receptivity, derogation, and intentions to mate-guard. Pers. Soc. Psychol. Bull. 40, 1260–1269 (2014).

    Article  PubMed  Google Scholar 

  70. Feinberg, D. R., DeBruine, L. M., Jones, B. C. & Perrett, D. I. The role of femininity and averageness of voice pitch in aesthetic judgments of women’s voices. Perception 37, 615–623 (2008).

    Article  PubMed  Google Scholar 

  71. Makhanova, A. & Miller, S. L. Female fertility and male mating: women’s ovulatory cues influence men’s physiology, cognition, and behavior. Soc. Personal. Psychol. Compass 7, 389–400 (2013).

    Article  Google Scholar 

  72. Miller, S. L. & Maner, J. K. Scent of a woman: men’s testosterone responses to olfactory ovulation cues. Psychol. Sci. 21, 276–283 (2010).

    Article  PubMed  Google Scholar 

  73. Puts, D. A. et al. Women’s attractiveness changes with estradiol and progesterone across the ovulatory cycle. Horm. Behav. 63, 13–19 (2013).

    Article  CAS  PubMed  Google Scholar 

  74. Doty, R. L., Ford, M., Preti, G. & Huggins, G. R. Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science 190, 1316–1318 (1975).

    Article  CAS  PubMed  Google Scholar 

  75. Kuukasjärvi, S. et al. Attractiveness of women’s body odors over the menstrual cycle: the role of oral contraceptives and receiver sex. Behav. Ecol. 15, 579–584 (2004).

    Article  Google Scholar 

  76. Roberts, S. C. et al. Female facial attractiveness increases during the fertile phase of the menstrual cycle. Proc. Biol. Sci. 271, S270–S272 (2004).

    Article  PubMed Central  Google Scholar 

  77. Silk, J. B., Alberts, S. C. & Altmann, J. Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim. Behav. 67, 573–582 (2004).

    Article  Google Scholar 

  78. Thornhill, R. et al. Major histocompatibility complex genes, symmetry, and body scent attractiveness in men and women. Behav. Ecol. 14, 668–678 (2003).

    Article  Google Scholar 

  79. Baenninger, M. A., Baenninger, R. & Houle, D. Attractiveness, attentiveness, and perceived male shortage: their influence on perceptions of other females. Evol. Hum. Behav. 14, 293–303 (1993).

    Google Scholar 

  80. Bullivant, S. B. et al. Women’s sexual experience during the menstrual cycle: identification of the sexual phase by noninvasive measurement of luteinizing hormone. J. Sex Res. 41, 82–93 (2004).

    Article  PubMed  Google Scholar 

  81. Cantú, S. M. et al. Fertile and selectively flirty: women’s behavior toward men changes across the ovulatory cycle. Psychol. Sci. 25, 431–438 (2014).

    Article  PubMed  Google Scholar 

  82. Dawson, S. J., Suschinsky, K. D. & Lalumière, M. L. Sexual fantasies and viewing times across the menstrual cycle: a diary study. Arch. Sex. Behav. 41, 173–183 (2012).

    Article  PubMed  Google Scholar 

  83. Durante, K. M., Griskevicius, V., Simpson, J. A., Cantú, S. M. & Li, N. P. Ovulation leads women to perceive sexy cads as good dads. J. Pers. Soc. Psychol. 103, 292–305 (2012).

    Article  PubMed  Google Scholar 

  84. Durante, K. M., Griskevicius, V., Hill, S. E., Perilloux, C. & Li, N. P. Ovulation, female competition, and product choice: hormonal influences on consumer behavior. J. Consum. Res. 37, 921–934 (2011).

    Article  Google Scholar 

  85. Durante, K. M., Li, N. P. & Haselton, M. G. Changes in women’s choice of dress across the ovulatory cycle: naturalistic and laboratory task-based evidence. Pers. Soc. Psychol. Bull. 34, 1451–1460 (2008).

    Article  PubMed  Google Scholar 

  86. Smith, M. J. L. et al. Facial appearance is a cue to oestrogen levels in women. Proc. Biol. Sci. 273, 135–140 (2006).

    CAS  PubMed  Google Scholar 

  87. Gangestad, S. W., Simpson, J. A., Cousins, A. J., Garver-Apgar, C. E. & Christensen, P. N. Women’s preferences for male behavioral displays change across the menstrual cycle. Psychol. Sci. 15, 203–207 (2004).

    Article  PubMed  Google Scholar 

  88. Gangestad, S. W., Garver-Apgar, C. E., Simpson, J. A. & Cousins, A. J. Changes in women’s mate preferences across the ovulatory cycle. J. Pers. Soc. Psychol. 92, 151–163 (2007).

    Article  PubMed  Google Scholar 

  89. Gangestad, S. W., Thornhill, R. & Garver-Apgar, C. E. Women’s sexual interests across the ovulatory cycle depend on primary partner developmental instability. Proc. R. Soc. Lond. B Biol. Sci. 272, 2023–2027 (2005).

    Google Scholar 

  90. Garver-Apgar, C. E., Gangestad, S. W. & Thornhill, R. Hormonal correlates of women’s mid-cycle preference for the scent of symmetry. Evol. Hum. Behav. 29, 223–232 (2008).

    Article  Google Scholar 

  91. Guéguen, N. Menstrual cycle phases and female receptivity to a courtship solicitation: an evaluation in a nightclub. Evol. Hum. Behav. 30, 351–355 (2009).

    Article  Google Scholar 

  92. Guéguen, N. Makeup and menstrual cycle: near ovulation, women use more cosmetics. Psychol. Rec. 62, 541–548 (2012).

    Article  Google Scholar 

  93. Guéguen, N. Gait and menstrual cycle: ovulating women use sexier gaits and walk slowly ahead of men. Gait Posture 35, 621–624 (2012).

    Article  PubMed  Google Scholar 

  94. Haselton, M. G., Mortezaie, M., Pillsworth, E. G., Bleske-Rechek, A. & Frederick, D. A. Ovulatory shifts in human female ornamentation: near ovulation, women dress to impress. Horm. Behav. 51, 40–45 (2007).

    Article  PubMed  Google Scholar 

  95. Maner, J. K. & McNulty, J. K. Attunement to the fertility status of same-sex rivals: women’s testosterone responses to olfactory ovulation cues. Evol. Hum. Behav. 34, 412–418 (2013).

    Article  Google Scholar 

  96. Lucas, M. & Koff, E. How conception risk affects competition and cooperation with attractive women and men. Evol. Hum. Behav. 34, 16–22 (2013).

    Article  Google Scholar 

  97. Lukaszewski, A. W. & Roney, J. R. Estimated hormones predict women’s mate preferences for dominant personality traits. Pers. Individ. Dif. 47, 191–196 (2009).

    Article  Google Scholar 

  98. Roney, J. R. & Simmons, Z. L. Women’s estradiol predicts preference for facial cues of men’s testosterone. Horm. Behav. 53, 14–19 (2008).

    Article  CAS  PubMed  Google Scholar 

  99. Roney, J. R. & Simmons, Z. L. Hormonal predictors of sexual motivation in natural menstrual cycles. Horm. Behav. 63, 636–645 (2013).

    Article  CAS  PubMed  Google Scholar 

  100. Roney, J. R., Simmons, Z. L. & Gray, P. B. Changes in estradiol predict within-women shifts in attraction to facial cues of men’s testosterone. Psychoneuroendocrinology 36, 742–749 (2011).

    Article  CAS  PubMed  Google Scholar 

  101. Piccoli, V., Foroni, F. & Carnaghi, A. Comparing group dehumanization and intra-sexual competition among normally ovulating women and hormonal contraceptive users. Pers. Soc. Psychol. Bull. 39, 1600–1609 (2013).

    Article  PubMed  Google Scholar 

  102. Pillsworth, E. G., Haselton, M. G. & Buss, D. M. Ovulatory shifts in female sexual desire. J. Sex. Res. 41, 55–65 (2004).

    Article  PubMed  Google Scholar 

  103. Saad, G. & Stenstrom, E. Calories, beauty, and ovulation: the effects of the menstrual cycle on food and appearance-related consumption. J. Consum. Psychol. 22, 102–113 (2012).

    Article  Google Scholar 

  104. Zhuang, J.-Y. & Wang, J.-X. Women ornament themselves for intrasexual competition near ovulation, but for intersexual attraction in luteal phase. PLoS ONE 9, e106407 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  105. Necka, E. A. et al. Women’s attention to and memory for fertile- and non-fertile phase women across the menstrual cycle.Adapt. Hum. Behav. Physiol. 4, 283–305 (2018).

    Article  Google Scholar 

  106. Necka, E. A., Puts, D. A., Dimitroff, S. J. & Norman, G. J. Other women’s fertility moderates female resource distribution across the menstrual cycle. Evol. Hum. Behav. 37, 387–391 (2016).

    Article  Google Scholar 

  107. Muller, M. N. & Wrangham, R. W. Sexual Coercion in Primates and Humans (Harvard Univ. Press, 2009).

  108. Bar-Tal, D. & Saxe, L. Physical attractiveness and its relationship to sex-role stereotyping. Sex Roles 2, 123–133 (1976).

    Article  Google Scholar 

  109. Buss, D. M. Sexual strategies theory: historical origins and current status. J. Sex Res. 35, 19–31 (1998).

    Article  Google Scholar 

  110. Liston, D. D. & Rahimi, R. in Geographies of Girlhood: Identities In-between (eds Bettis, P. J. & Adams, N. G.) 211–230 (Routledge, 2005).

  111. Baumeister, R. F., Bratslavsky, E., Finkenauer, C. & Vohs, K. D.Bad is stronger than good. Rev. Gen. Psychol. 5, 323–370 (2001).

    Article  Google Scholar 

  112. Hess, N. C. & Hagen, E. Informational Warfare: The Evolution of Female Coalitions and Gossip (Univ. California, 2006).

  113. Hess, N. H. Informational warfare: coalitional gossiping as a strategy for within-group aggression. in The Oxford Handbook of Women and Competition (ed. Fisher, M. L.) 223–246 (Oxford Univ. Press, 2017).

  114. Cohen, J. A power primer. Psychol. Bull. 112, 155–159 (1992).

    Article  CAS  PubMed  Google Scholar 

  115. Treas, J. & Giesen, D. Sexual infidelity among married and cohabiting Americans. J. Marriage Fam. 62, 48–60 (2000).

    Article  Google Scholar 

  116. Seal, D. W., Agostinelli, G. & Hannett, C. A. Extradyadic romantic involvement: moderating effects of sociosexuality and gender. Sex Roles 31, 1–22 (1994).

    Article  Google Scholar 

  117. Blow, A. J. & Hartnett, K. Infidelity in committed relationships I: a methodological review. J. Marital Fam. Ther. 31, 183–216 (2005).

    Article  PubMed  Google Scholar 

  118. Dorjahn, V. R. The factor of polygyny in African demography. in Continuity and Change in African Cultures (eds. Bascom, W. R. & Herskovits., M. J.) 87–112 (Univ. Chicago Press, 1959).

  119. Goody, J. Polygyny, economy, and the role of women. in The Character of Kinship (ed. Goody, J.) 175–190 (Cambridge Univ. Press, 1973).

  120. Baumeister, R. F. & Vohs, K. D. Sexual economics: sex as female resource for social exchange in heterosexual interactions. Pers. Soc. Psychol. Rev. 8, 339–363 (2004).

    Article  PubMed  Google Scholar 

  121. Benenson, J. F. et al. Social exclusion: more important to human females than males. PLoS ONE 8, e55851 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. McAndrew, F. T. & Milenkovic, M. A. Of tabloids and family secrets: the evolutionary psychology of gossip. J. Appl. Soc. Pyschol. 32, 1064–1082 (2002).

    Article  Google Scholar 

  123. Fernandez-Duque, E., Valeggia, C. R. & Mendoza, S. P. The biology of paternal care in human and nonhuman primates. Annu. Rev. Anthropol. 38, 115–130 (2009).

    Article  Google Scholar 

  124. Buss, D. M. & Schmitt, D. P. Sexual strategies theory: an evolutionary perspective on human mating. Psychol. Rev. 100, 204–232 (1993).

    Article  CAS  PubMed  Google Scholar 

  125. Scelza, B. A. et al. Patterns of paternal investment predict cross-cultural variation in jealous response. Nat. Hum. Behav. 4, 20–26 (2020).

    Article  PubMed  Google Scholar 

  126. Greiling, H. & Buss, D. M. Women’s sexual strategies: the hidden dimension of extra-pair mating. Pers. Individ. Dif. 28, 929–963 (2000).

    Article  Google Scholar 

  127. Schmitt, D. P. Sociosexuality from Argentina to Zimbabwe: a 48-nation study of sex, culture, and strategies of human mating. Behav. Brain Sci. 28, 247–275 (2005).

    Article  PubMed  Google Scholar 

  128. Anderson, K. G. How well does paternity confidence match actual paternity? Evidence from worldwide nonpaternity rates. Curr. Anthropol. 47, 513–520 (2006).

    Article  Google Scholar 

  129. Scelza, B. A. Female choice and extra-pair paternity in a traditional human population. Biol. Lett. 7, 889–891 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  130. Wiessner, P. Parent–offspring conflict in marriage: implications for social evolution and material culture among the Ju/’Hoansi bushmen. in Pattern and Process in Cultural Evolution (ed. Shennan, S.) 251–263 (Univ. California Press, 2009).

  131. Starkweather, K. E. & Hames, R. A survey of non-classical polyandry. Hum. Nat. 23, 149–172 (2012).

    Article  PubMed  Google Scholar 

  132. Schmitt, D. P. & Rohde, P. A. The human polygyny index and its ecological correlates: testing sexual selection and life history theory at the cross-national level. Soc. Sci. Q. 94, 1159–1184 (2013).

    Article  Google Scholar 

  133. Vervaecke, H., Stevens, J. & Van Elsacker, L. Interfering with others: female–female reproductive competition in Pan paniscus. in Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions (ed. Jones, C. B.) 231–253 (American Society of Primatologists, 2003).

  134. Haselton, M. G. & Gildersleeve, K. Human ovulation cues. Curr. Opin. Psychol. 7, 120–125 (2016).

    Article  Google Scholar 

  135. Wilensky, U. NetLogo (Center for Connected Learning and Computer-Based Modeling, Northwestern Univ., 1999).

  136. Dunbar, R. I. M. Coevolution of neocortical size, group size and language in humans. Behav. Brain Sci. 16, 681–694 (1993).

    Article  Google Scholar 

  137. Marlowe, F. W. Hunter-gatherers and human evolution. Evol. Anthropol. 14, 54–67 (2005).

    Article  Google Scholar 

  138. Sear, R. & Mace, R. Who keeps children alive? A review of the effects of kin on child survival. Evol. Hum. Behav. 29, 1–18 (2008).

    Article  Google Scholar 

  139. Broekmans, F. J., Knauff, E. A. H., te Velde, E. R., Macklon, N. S. & Fauser, B. C. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol. Metab. 18, 58–65 (2007).

    Article  CAS  PubMed  Google Scholar 

  140. R Core Development Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016).

  141. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).

  142. Beall, A. T. & Schaller, M. Affective implications of the mating/parenting trade-off: short-term mating motives and desirability as a short-term mate predict less intense tenderness responses to infants. Pers. Individ. Dif. 68, 112–117 (2014).

    Article  Google Scholar 

  143. Gangestad, S. W. & Simpson, J. A. The evolution of human mating: trade-offs and strategic pluralism. Behav. Brain Sci. 23, 573–587 (2000).

    Article  CAS  PubMed  Google Scholar 

  144. Kaplan, H. S. & Gangestad, S. W. Life history theory and evolutionary psychology. in The Handbook of Evolutionary Psychology (ed. Buss, D.) 68–95 (Wiley, 2005).

  145. Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, 1992).

  146. Bisdee, J. T., James, W. P. & Shaw, M. A. Changes in energy expenditure during the menstrual cycle. Br. J. Nutr. 61, 187–199 (1989).

    Article  CAS  PubMed  Google Scholar 

  147. Jasienska, G. The Fragile Wisdom: An Evolutionary View on Women’s Biology and Health (Harvard Univ. Press, 2013).

  148. Price, P. N., Duncan, S. L. & Levin, R. J. Oxygen consumption of human endometrium during the menstrual cycle measured in vitro using an oxygen electrode. J. Reprod. Fertil. 63, 185–192 (1981).

    Article  CAS  PubMed  Google Scholar 

  149. Manocha, S., Choudhuri, G. & Tandon, B. N. A study of dietary intake in pre- and post-menstrual period. Hum. Nutr. Appl. Nutr. 40, 213–216 (1986).

    CAS  PubMed  Google Scholar 

  150. Webb, P. 24-hour energy expenditure and the menstrual cycle. Am. J. Clin. Nutr. 44, 614–619 (1986).

    Article  CAS  PubMed  Google Scholar 

  151. Ellison, P. T., Panter-Brick, C., Lipson, S. F. & O’Rourke, M. T. The ecological context of human ovarian function. Hum. Reprod. 8, 2248–2258 (1993).

    Article  CAS  PubMed  Google Scholar 

  152. Kramer, P. A. The costs of human locomotion: maternal investment in child transport. Am. J. Phys. Anthropol. 107, 71–85 (1998).

    Article  CAS  PubMed  Google Scholar 

  153. Cantoni, D. & Brown, R. E. Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Anim. Behav. 54, 377–386 (1997).

    Article  CAS  PubMed  Google Scholar 

  154. Lunn, P. G., Austin, S., Prentice, A. M. & Whitehead, R. G. The effect of improved nutrition on plasma prolactin concentrations and postpartum infertility in lactating Gambian women. Am. J. Clin. Nutr. 39, 227–235 (1984).

    Article  CAS  PubMed  Google Scholar 

  155. Mitani, J. C. & Watts, D. The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav. Ecol. Sociobiol. 40, 213–220 (1997).

    Article  Google Scholar 

  156. Gettler, L. T. Direct male care and hominin evolution: why male–child interaction is more than a nice social idea. Am. Anthropol. 112, 7–21 (2010).

    Article  Google Scholar 

  157. Miller, G., Tybur, J. M. & Jordan, B. D. Ovulatory cycle effects on tip earnings by lap dancers: economic evidence for human estrus? Evol. Hum. Behav. 28, 375–381 (2007).

    Article  Google Scholar 

  158. Wilcox, A. J., Dunson, D. B., Weinberg, C. R., Trussell, J. & Baird, D. D. Likelihood of conception with a single act of intercourse: providing benchmark rates for assessment of post-coital contraceptives. Contraception 63, 211–215 (2001).

    Article  CAS  PubMed  Google Scholar 

  159. Betzig, L. Causes of conjugal dissolution: a cross-cultural study. Curr. Anthropol. 30, 654–676 (1989).

    Article  Google Scholar 

  160. Davies, A. P. C., Shackelford, T. K. & Hass, R. G. Sex differences in perceptions of benefits and costs of mate poaching. Pers. Individ. Dif. 49, 441–445 (2010).

    Article  Google Scholar 

  161. Perlini, A. H. & Boychuk, T. L. Social influence, desirability and relationship investment: the effects of resourcefulness and sexual permissiveness. Soc. Behav. Pers. 34, 593–602 (2006).

    Article  Google Scholar 

  162. Buss, D. M. Sex differences in human mate preferences: evolutionary hypotheses tested in 37 cultures. Behav. Brain Sci. 12, 1–14 (1989).

    Article  Google Scholar 

  163. Buss, D. M. Sexual strategies: a journey into controversy. Psychol. Inq. 14, 219–226 (2003).

    Article  Google Scholar 

  164. Cashdan, E. Attracting mates: effects of paternal investment on mate attraction strategies. Ethol. Sociobiol. 14, 1–23 (1993).

    Article  Google Scholar 

  165. Simpson, J. A. & Gangestad, S. W. Sociosexuality and romantic partner choice. J. Pers. 60, 31–51 (1992).

    Article  Google Scholar 

  166. Draper, P. & Harpending, H. Father absence and reproductive strategy: an evolutionary perspective. J. Anthropol. Res. 38, 255–273 (1982).

    Article  Google Scholar 

  167. Werner, N. E. & Crick, N. R. Relational aggression and social-psychological adjustment in a college sample. J. Abnorm. Psychol. 108, 615–623 (1999).

    Article  CAS  PubMed  Google Scholar 

  168. Archer, J. & Coyne, S. M. An integrated review of indirect, relational, and social aggression. Pers. Soc. Psychol. Rev. 9, 212–230 (2005).

    Article  PubMed  Google Scholar 

  169. Hamilton, M. J., Milne, B. T., Walker, R. S., Burger, O. & Brown, J. H. The complex structure of hunter–gatherer social networks. Proc. R. Soc. B Biol. Sci. 274, 2195–2203 (2007).

    Article  Google Scholar 

  170. Bird, D. W., Bird, R. B., Codding, B. F. & Zeanah, D. W. Variability in the organization and size of hunter-gatherer groups: foragers do not live in small-scale societies. J. Hum. Evol. 131, 96–108 (2019).

    Article  PubMed  Google Scholar 

  171. Hill, K. R., Wood, B. M., Baggio, J., Hurtado, A. M. & Boyd, R. T. Hunter-gatherer inter-band interaction rates: implications for cumulative culture. PLoS ONE 9, e102806 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  172. Hill, R. A., Bentley, R. A. & Dunbar, R. I. M. Network scaling reveals consistent fractal pattern in hierarchical mammalian societies. Biol. Lett. 4, 748–751 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  173. Dunbar, R. I. M. & Sosis, R. Optimising human community sizes. Evol. Hum. Behav. 39, 106–111 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  174. Lehmann, J., Lee, P. C. & Dunbar, R. I. M. Unravelling the function of community-level organization. in Lucy to Language: The Benchmark Papers (eds. Dunbar, R. I. M., Gamble, C. & Gowlett, J. A. J.) 245–276 (Oxford Univ. Press, 2014).

Download references

Acknowledgements

The authors received no specific funding for this work.

Author information

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

Authors
  1. Jaimie Arona Krems
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Scott Claessens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Melissa R. Fales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marco Campenni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martie G. Haselton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Athena Aktipis
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Athena Aktipis.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Primary Handling Editor: Aisha Bradshaw.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Supplementary information

Supplementary Information

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

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41562-020-01038-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing