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Evolutionary Psychological Science

, Volume 4, Issue 2, pp 179–190 | Cite as

Disgust, Sexual Cues, and the Prophylaxis Hypothesis

  • Amanda D. Timmers
  • Jennifer A. Bossio
  • Meredith L. ChiversEmail author
Research Article

Abstract

Women’s susceptibility to infection has been found to vary across the menstrual cycle. During the luteal phase of the menstrual cycle, when progesterone levels are at their peak, women experience a downregulation in inflammatory immune responses to tolerate the presence of foreign paternal genetic material. The prophylaxis hypothesis holds that, during such periods of physiological immune vulnerability, women will engage in increased prophylactic behavior in response to cues associated with pathogen transmission (like sexual cues) to guard against infection. The current study examined disgust and other proposed prophylactic responses (i.e., attention and desire for solitary and dyadic sexual activity) in response to sexual and nonsexual films among naturally cycling women (N = 21) during the follicular and luteal phases of their menstrual cycles. No significant differences were found during the follicular and luteal phase on disgust, attention, or desire for solitary or dyadic sexual activity. Strong negative associations were found between feelings of disgust to sexual stimuli and proposed prophylactic behaviors (attention, desire for sexual activity with a partner) that were most prominent during the luteal phase of women’s menstrual cycles, suggesting that they may have served as a prophylactic mechanism, protecting women’s bodies from infection during a period of immune vulnerability. However, contrary to hypothesis, no significant associations were found between progesterone (the hormone that regulates changes in immune functioning) and proposed prophylactic responses. Further research examining prophylactic effects in response to sexual stimuli is warranted.

Keywords

Disgust Menstrual cycle Progesterone Sex Prophylaxis 

Notes

Acknowledgments

Many thanks are given to the study participants for their invaluable assistance in completing this study.

Funding Information

This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada (Grant No. 386198-10) and the Queen’s Senate Advisory Research Council, awarded to M. L. Chivers and an Ontario Women’s Health Scholar Award (funded by the Ministry of Health and Long Term Care) and a Social Sciences and Humanities Research Council of Canada Joseph Armand Bombardier Canada Graduate Scholarship awarded to the first author.

Compliance with Ethical Standards

Study procedures were approved by our Health Sciences and Affiliated Teaching Hospitals Research Ethics Board. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. Alexander, N. J. (1990). Sexual transmission of human immunodeficiency virus: virus entry into the male and female genital tract. Fertility and Sterility, 54(1), 1–18.CrossRefPubMedGoogle Scholar
  2. Andrews III, A. R., Crone, T., Cholka, C. B., Cooper, T. V., & Bridges, A. J. (2015). Correlational and experimental analyses of the relation between disgust and sexual arousal. Motivation and Emotion.  https://doi.org/10.1007/s11031-015-9485-y.
  3. Angyal, A. (1941). Disgust and related aversions. The Journal of Abnormal and Social Psychology, 36(3), 393.CrossRefGoogle Scholar
  4. Bakos, O., Lundkvist, L., Wide, O., & Bergh, T. (1994). Ultrasonographical and hormonal description of the normal ovulatory menstrual cycle. Acta Obstetrica et Gynecologica Scandanavica, 73, 790–796.CrossRefGoogle Scholar
  5. Bancroft, J., Graham, C. A., Janssen, E., & Sanders, S. A. (2009). The dual control model: current status and future directions. Journal of Sex Research, 46(2–3), 121–142.CrossRefPubMedGoogle Scholar
  6. Borg, C., & de Jong, P. J. (2012). Feelings of disgust and disgust-induced avoidance weaken following induced sexual arousal in women. PLoS One, 7(9), e44111.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Borg, C., de Jong, P. J., & Georgiadis, J. R. (2014). Subcortical BOLD responses during visual sexual stimulation vary as a function of implicit porn associations in women. Social Cognitive and Affective Neuroscience, 9(2), 158–166.CrossRefPubMedGoogle Scholar
  8. Bossio, J. A., Suschinsky, K. D., Puts, D. A., & Chivers, M. L. (2014). Does menstrual cycle phase influence the gender specificity of heterosexual women’s genital and subjective sexual arousal? Archives of Sexual Behavior, 43(5), 941–952.CrossRefPubMedGoogle Scholar
  9. Both, S., Everaerd, W., & Laan, E. (2007). Desire emerges from excitement. A psychophysiological perspective on sexual motivation. In E. Janssen (Ed.), The psychophysiology of sex (pp. 327–339). Bloomington: Indiana University Press.Google Scholar
  10. Chakraborty, H., Sen, P. K., Helms, R. W., Vernazza, P. L., Fiscus, S. A., Eron, J. J., et al. (2001). Viral burden in genital secretions determines male-to-female sexual transmission of HIV-1: a probabilistic empiric model. AIDS, 15(5), 621–627.CrossRefPubMedGoogle Scholar
  11. Chiazze, L., Brayer, F. T., MacIsco, J. J., Parker, M. P., & Duffy, B. J. (1968). The length and variability of the human menstrual cycle. Journal of the American Medical Association, 203, 377–380.CrossRefPubMedGoogle Scholar
  12. Chivers, M. L., Rieger, G., Latty, E., & Bailey, J. M. (2004). A sex difference in the specificity of sexual arousal. Psychological Science, 15, 736–744.CrossRefPubMedGoogle Scholar
  13. Chivers, M. L., Seto, M. C., & Blanchard, R. (2007). Gender and sexual orientation differences in sexual response to sexual activities versus gender of actors in sexual films. Journal of Personality and Social Psychology, 93, 1108–1121.CrossRefPubMedGoogle Scholar
  14. Clark, W. R. (2007). In defense of self: how the immune system really works in managing health and disease. Oxford: Oxford University Press.Google Scholar
  15. Conway, C. A., Jones, B. C., DeBruine, L. M., Welling, L. L. M., Smith, M. L., Perrett, D. I., et al. (2007). Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Hormones and Behaviour, 51(2), 202–206.CrossRefGoogle Scholar
  16. Corner, G. W., & Allen, W. M. (1929). Physiology of the corpus luteum. II. Production of a special uterine reaction (progestational proliferation) by extracts of the corpus luteum. American Journal of Physiology, 88(2), 326–339.Google Scholar
  17. Critchley, H. O., Kelly, R. W., Brenner, R. M., & Baird, D. T. (2001). The endocrinology of menstruation—a role for the immune system. Clinical Endocrinology, 55(6), 701–710.CrossRefPubMedGoogle Scholar
  18. Curtis, V., Aunger, R., & Rabie, T. (2004). Evidence that disgust evolved to protect from risk of disease. Proceedings of the Royal Society Biological Sciences, 271, 131–133.CrossRefGoogle Scholar
  19. Darwin, C. (1965). The expression of emotions in man and animal. Chicago: University of Chicago Press (Original work published 1872).Google Scholar
  20. Dawson, S. J., & Chivers, M. L. (2014). Gender-specificity of solitary and dyadic sexual desire among gynephilic and androphilic women and men. The Journal of Sexual Medicine, 11(4), 980–994.CrossRefPubMedGoogle Scholar
  21. de Jong, P. J., & Peters, M. L. (2007). Contamination vs. harm-relevant outcome expectancies and covariation bias in spider phobia. Behaviour Research and Therapy, 45, 1271–1284.CrossRefPubMedGoogle Scholar
  22. de Jong, P. J., van Overveld, M., & Borg, C. (2013). Giving in to arousal or staying stuck in disgust? Disgust-based mechanisms in sex and sexual dysfunction. Journal of Sex Research, 50(3–4), 247–262.CrossRefPubMedGoogle Scholar
  23. Dillon, K. M., & Brooks, D. (1992). Unusual cleaning behaviour in the luteal phase. Psychological Reports, 70(1), 35.CrossRefPubMedGoogle Scholar
  24. Ekman, P., & Friesen, W. V. (1971). Constants across cultures in the face and emotion. Journal of Personality and Social Psychology, 17(2), 124.CrossRefPubMedGoogle Scholar
  25. Ekman, P., & Friesen, W. V. (1986). A new pan-cultural facial expression of emotion. Motivation and Emotion, 10(2), 159–168.CrossRefGoogle Scholar
  26. Ekman, P., Levenson, R. W., & Friesen, W. V. (1983). Autonomic nervous system activity distinguishes among emotions. Science, 221(4616), 1208–1210.CrossRefPubMedGoogle Scholar
  27. Ellison, P. T. (1988). Human salivary steroids: methodological considerations and applications in physical anthropology. American Journal of Physical Anthropology, 31(S9), 115–142.CrossRefGoogle Scholar
  28. Fessler, D. M. (2001). Luteal phase immunosuppression and meat eating. Rivista di Biologia Biology Forum, 94(3), 403–426.PubMedGoogle Scholar
  29. Fessler, D. T. (2002). Reproductive immunosuppression and diet. Current Anthropology, 43(1), 19–61.CrossRefPubMedGoogle Scholar
  30. Fessler, D. M., & Navarrete, C. D. (2003). Domain-specific variation in disgust sensitivity across the menstrual cycle. Evolution and Human Behavior, 24(6), 406–417.CrossRefGoogle Scholar
  31. Fessler, D. M. T., Pillsworth, E. G., & Flamson, T. J. (2004). Angry men and disgusted women: an evolutionary approach to the influence of emotions on risk taking. Organizational Behaviour and Human Decision Processes, 95, 107–123.CrossRefGoogle Scholar
  32. Fessler, D. M., Eng, S. J., & Navarrete, C. D. (2005). Elevated disgust sensitivity in the first trimester of pregnancy: evidence supporting the compensatory prophylaxis hypothesis. Evolution and Human Behavior, 26(4), 344–351.CrossRefGoogle Scholar
  33. Flaxman, S. M., & Sherman, P. W. (2000). Morning sickness: a mechanism for protecting mother and embryo. The Quarterly Review of Biology, 75, 113–148.CrossRefPubMedGoogle Scholar
  34. Fleischman, D. S. (2014). Women’s disgust adaptations. In Evolutionary perspectives on human sexual psychology and behavior (pp. 277–296). New York: Springer.Google Scholar
  35. Fleischman, D. S., & Fessler, D. M. T. (2011). Progesterone’s effects on the psychology of disease avoidance: support for the compensatory behavioural prophylaxis hypothesis. Hormones and Behaviour, 59(2), 271–275.CrossRefGoogle Scholar
  36. Fleischman, D. S., Hamilton, L. D., Fessler, D. M., & Meston, C. M. (2015). Disgust versus lust: exploring the interactions of disgust and fear with sexual arousal in women. PLoS One, 10(6), e0118151.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fumagalli, M., Sironi, M., Pozzoli, U., Ferrer-Admetlla, A., Pattini, L., & Nielsen, R. (2011). Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure throughout human evolution. PLoS Genetics, 7, e1002355.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gangestad, S. W. (2007). Reproductive strategies and tactics. In R. I. M. Dunbar & L. Barrett (Eds.), Oxford handbook of evolutionary psychology (pp. 321–332). Oxford: Oxford University Press.Google Scholar
  39. Gangestad, S. W., & Haselton, M. G. (2015). Human estrus: implications for relationship science. Current Opinion in Psychology, 1, 45–51.CrossRefGoogle Scholar
  40. Geer, J. H., & Bellard, H. S. (1996). Sexual content induced delays in unprimed lexical decisions: gender and context effects. Archives of Sexual Behavior, 25, 379–395.CrossRefPubMedGoogle Scholar
  41. Gildersleeve, K., Haselton, M. G., & Fales, M. R. (2014). Do women’s mate preferences change across the ovulatory cycle? A meta-analytic review. Psychological Bulletin, 140(5), 1205–1259.CrossRefPubMedGoogle Scholar
  42. Haidt, J., McCauley, C., & Rozin, P. (1994). Individual differences in sensitivity to disgust: a scale sampling seven domains of disgust elicitors. Personality and Individual Differences, 16, 701–713.CrossRefGoogle Scholar
  43. Hyde, J. S., DeLamater, J. D., & Byers, E. S. (2004). Understanding human sexuality: third Canadian edition. Toronto: McGraw-Hill Ryerson.Google Scholar
  44. Janssen, E., Everaerd, W., Spiering, M., & Janssen, J. (2000). Automatic processes and the appraisal of sexual stimuli: toward an information processing model of sexual arousal. Journal of Sex Research, 37, 8–23.CrossRefGoogle Scholar
  45. Jones, B. C., Little, A. C., Boothroyd, L., DeBruine, L. M., Feinberg, D. R., Law Smith, M. J., et al. (2005). Commitment to relationships and preferences for femininity and apparent health in faces are strongest on days of the menstrual cycle when progesterone level is high. Hormones and Behaviour, 48, 283–290.CrossRefGoogle Scholar
  46. Jones, B. C., Hahn, A. C., Fisher, C. I., Wang, H., Kandrik, M., Han, C., … DeBruine, L. M. (2017). Women’s preferences for facial masculinity are not related to their hormonal status. bioRxiv. Preprint retrieved from http://biorxiv.org/content/early/2017/05/11/136549.
  47. Karama, S., Armony, J., & Beauregard, M. (2011). Film excerpts shown to specifically elicit various affects lead to overlapping activation foci in a large set of symmetrical brain regions in males. PLoS One, 6(7), e22343.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kelly, D. R. (2011). Yuck!: the nature and moral significance of disgust. Cambridge: MIT Press.Google Scholar
  49. Kinsey, A. C., Pomeroy, W. B., Martin, C. E., & Gebhard, P. H. (1953). Sexual behavior in the human female. Philadelphia: Saunders.Google Scholar
  50. Koukounas, E., & McCabe, M. P. (1997). Sexual and emotional variables influencing sexual response to erotica. Behaviour Research and Therapy, 35(3), 221–231.CrossRefPubMedGoogle Scholar
  51. Laskin, D. L., Sunil, V. R., Gardner, C. R., & Laskin, J. D. (2011). Macrophages and tissue injury: agents of defense or destruction? Annual Review of Pharmacology and Toxicology, 51, 267–288.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lee, E. M., Ambler, J. K., & Sagarin, B. J. (2014). Effects of subjective sexual arousal on sexual, pathogen, and moral disgust sensitivity in women and men. Archives of Sexual Behavior, 43, 1115–1121.CrossRefPubMedGoogle Scholar
  53. Liu, Y., Zhang, D., & Luo, Y. (2014). How disgust facilitates avoidance: an ERP study on attention modulation by threats. Social Cognitive and Affective Neuroscience, 10(4), 598–604.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lochmiller, R. L., & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87–98.CrossRefGoogle Scholar
  55. Madkan, V. K., Giancola, A. A., Sra, K. K., & Tyring, S. K. (2006). Sex differences in the transmission, prevention, and disease manifestations of sexually transmitted diseases. Archives of Dermatology, 142(3), 365–370.CrossRefPubMedGoogle Scholar
  56. Meston, C. M., & Frohlich, P. F. (2000). The neurobiology of sexual function. Archives of General Psychiatry, 57, 1012–1030.CrossRefPubMedGoogle Scholar
  57. Morokoff, P. J. (1986). Volunteer bias in the psychophysiological study of female sexuality. Journal of Sex Research, 22(1), 35–51.CrossRefGoogle Scholar
  58. Nallanathan, B., Mendoza, K., Curran, M.J., Lindau, S.T. (2007). Salivary progesterone measurement in wave I of the National Social Life, Health & Aging Project (NSHAP). Chicago Core on Biomarkers in Population-Based Aging Research (http://biomarkers.uchicago.edu/pdfs/TR-Progesterone.pdf).
  59. Oaten, M., Stevenson, R. J., & Case, T. L. (2009). Disgust as a disease-avoidance mechanism. Psychological Bulletin, 135, 303–321.CrossRefPubMedGoogle Scholar
  60. Olatunji, B. O., Huijding, J., de Jong, P. G., & Smits, J. A. J. (2011). The relative contributions of fear and disgust reductions to improvements in spider phobia following exposure-based treatment. Journal of Behavior Therapy and Experimental Psychiatry, 42, 117–121.CrossRefPubMedGoogle Scholar
  61. Panter-Brick, C., Lotstein, D. S., & Ellison, P. T. (1993). Seasonality of reproductive function and weight loss in rural Nepali women. Human Reproduction, 8(5), 684–690.CrossRefPubMedGoogle Scholar
  62. Plutchik, R. (1962). The emotions: facts, theories, and a new model. New York: Random House.Google Scholar
  63. Puts, D. A. (2006). Cyclic variation in women’s preferences for masculine traits. Human Nature, 17, 114–127.CrossRefPubMedGoogle Scholar
  64. Quigley, J. F., Sherman, M. F., & Sherman, N. C. (1997). Personality disorder symptoms, gender, and age as predictors of adolescent disgust sensitivity. Personality and Individual Differences, 22(5), 661–667.CrossRefGoogle Scholar
  65. Regan, P. C. (1996). Rhythms of desire: the association between menstrual cycle phases and female sexual desire. Canadian Journal of Human Sexuality, 5, 145–156.Google Scholar
  66. Rohrmann, S., & Hopp, H. (2008). Cardiovascular indicators of disgust. International Journal of Psychophysiology, 68(3), 201–208.CrossRefPubMedGoogle Scholar
  67. Rozin, P., & Fallon, A. E. (1987). A perspective on disgust. Psychological Review, 94(1), 23–41.CrossRefPubMedGoogle Scholar
  68. Rozin, P., Nemeroff, C., Horowitz, M., Gordon, B., & Voet, W. (1995). The borders of the self: contamination sensitivity and potency of the body apertures and other body parts. Journal of Research in Personality, 29, 318–340.CrossRefGoogle Scholar
  69. Rozin, P., Haidt, J., & McCauley, C. R. (2000). Disgust. In M. Lewis & J. M. Haviland (Eds.), Handbook of emotions. New York: Guilford Publications.Google Scholar
  70. Spape, J., Timmers, A. D., Yoon, S., Ponseti, J., & Chivers, M. L. (2014). Gender-specific genital and subjective sexual arousal to prepotent sexual features in heterosexual women and men. Biological Psychology, 102, 1–9.CrossRefPubMedGoogle Scholar
  71. Spector, I. P., Carey, M. P., & Steinberg, L. (1996). The sexual desire inventory: development, factor structure, and evidence of reliability. Journal of Sex & Marital Therapy, 22(3), 175–190.CrossRefGoogle Scholar
  72. Spiering, M., Everaerd, W., & Laan, E. (2004). Conscious processing of sexual information: mechanisms of appraisal. Archives of Sexual Behavior, 33, 369–380.  https://doi.org/10.1023/B:ASEB.0000028890.08687.94.CrossRefPubMedGoogle Scholar
  73. Strassberg, D. S., & Lowe, K. (1995). Volunteer bias in sexuality research. Archives of Sexual Behavior, 24(4), 369–382.CrossRefPubMedGoogle Scholar
  74. Twenge, J. M., Sherman, R. A., & Wells, B. E. (2017). Declines in sexual frequency among American adults, 1989–2014. Archives of Sexual Behavior, 1–13.Google Scholar
  75. Tybur, J. M., Lieberman, D., & Griskevicius, V. (2009). Microbes, mating, and morality: Individual differences in three functional domains of disgust. Journal of Personality and Social Psychology, 97, 103–122.CrossRefPubMedGoogle Scholar
  76. Tybur, J. M., Bryan, A. D., Lieberman, D., Hooper, A. E. C., & Merriman, L. A. (2011). Sex differences and sex similarities in disgust sensitivity. Personality and Individual Differences, 51(3), 343–348.CrossRefGoogle Scholar
  77. van Overveld, M., & Borg, C. (2015). Brief emotion regulation training facilitates arousal control during sexual stimuli. The Journal of Sex Research, 52(9), 996–1005.CrossRefPubMedGoogle Scholar
  78. Vitzthum, V. J., Bentley, G. R., Spielvogel, H., Caceres, E., Thornburg, J., Jones, L., Shore, S., Hodges, K. R., & Chatterton, R. T. (2002). Salivary progesterone levels and rate of ovulation are significantly lower in poorer than in better-off urban-dwelling Bolivian women. Human Reproduction, 17(7), 1906–1913.CrossRefPubMedGoogle Scholar
  79. Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron, 30, 829–841.CrossRefPubMedGoogle Scholar
  80. Wilcox, A. J., Dunson, D. B., Weinberg, C. R., Trussell, J., & Baird, D. D. (2001). Likelihood of conception with a single act of intercourse: providing benchmark rates for assessment of post-coital contraceptives. Contraception, 63(4), 211–215.CrossRefPubMedGoogle Scholar
  81. Woody, S. R., McLean, C., & Klassen, T. (2005). Disgust as a motivator of avoidance of spiders. Journal of Anxiety Disorders, 19, 461–475.CrossRefPubMedGoogle Scholar
  82. Żelaźniewicz, A., Borkowska, B., Nowak, J., & Pawłowski, B. (2016). The progesterone level, leukocyte count and disgust sensitivity across the menstrual cycle. Physiology & Behavior, 161, 60–65.CrossRefGoogle Scholar
  83. Zsok, F., Fleischman, D. S., Borg, C., & Morrison, E. (2017). Disgust trumps lust: women’s disgust and attraction towards men is unaffected by sexual arousal. Evolutionary Psychological Science, 1–11.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Amanda D. Timmers
    • 1
  • Jennifer A. Bossio
    • 2
  • Meredith L. Chivers
    • 1
    Email author
  1. 1.Department of PsychologyQueen’s UniversityKingstonCanada
  2. 2.Department of Obstetrics and GynaecologyUniversity of British ColumbiaVancouverCanada

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