Abstract
There is growing evidence that steroid hormones interact to shape social behavior. In particular, regarding basal hormonal levels, cortisol has repeatedly been found to moderate the effect of testosterone on behavior. However, the role of contextual and hormone-altering factors such as acute stress on dual-hormone associations is largely unknown. In the present study, we aimed to evaluate whether baseline testosterone and cortisol levels predict dominance- and friendliness-related social behavior. Additionally, we focused on the moderating role of acute stress. In a laboratory study, 42 female and 38 male participants were allocated to same-sex dyads. Each dyad member was randomly assigned to a stress or control condition. Subsequently, the dyads performed a competitive role-play. Salivary cortisol, testosterone and mood levels were repeatedly assessed. Social behavior (dominance and friendliness) was rated based on the videotaped role-plays. For the combined sample of men and women in the stress condition, we found a negative relation between basal testosterone levels and friendliness, but only when basal cortisol levels were low. Interactions between testosterone and cortisol responses did not predict social behavior. In conclusion, our findings provide first evidence for the dual-hormone hypothesis in the context of interpersonal theory and reinforce the relevance of considering contextual factors such as acute stress.
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References
Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park: Sage Publications.
Akinola, M., Page-Gould, E., Mehta, P. H., & Lu, J. G. (2016). Collective hormonal profiles predict group performance. Proceedings of the National Academy of Sciences, 113(35), 9774–9779. doi:10.1073/pnas.1603443113.
Antons, K., & Volmerg, U. (2000). Praxis der Gruppendynamik: Übungen und Techniken (8th ed.). Göttingen: Hogrefe.
Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30(3), 319–345. doi:10.1016/j.neubiorev.2004.12.007.
Barton, K. (2016). Package “MuMln.” Retrieved February 10, 2016, from https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf.
Bates, D., & Mächler, M. (2016). Package “lme4.” Retrieved March 14, 2016, from https://cran.r-project.org/web/packages/lme4/lme4.pdf. Accessed 14 March 2016.
Bedgood, D., Boggiano, M. M., & Turan, B. (2014). Testosterone and social evaluative stress: The moderating role of basal cortisol. Psychoneuroendocrinology, 47, 107–115. doi:10.1016/j.psyneuen.2014.05.007.
Bos, P. A., Panksepp, J., Bluthé, R.-M., & van Honk, J. (2012). Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies. Frontiers in Neuroendocrinology, 33(1), 17–35. doi:10.1016/j.yfrne.2011.01.002.
van den Bos, W., Golka, P. J. M., Effelsberg, D., & McClure, S. M. (2013). Pyrrhic victories: The need for social status drives costly competitive behavior. Frontiers in Neuroscience, 7(7 OCT), 1–11. doi:10.3389/fnins.2013.00189.
Campbell, J., & Ehlert, U. (2012). Acute psychosocial stress: Does the emotional stress response correspond with physiological responses? Psychoneuroendocrinology, 37(8), 1111–1134. doi:10.1016/j.psyneuen.2011.12.010.
Carré, J. M., & Mehta, P. H. (2011). Importance of considering testosterone-cortisol interactions in predicting human aggression and dominance. Aggressive Behavior, 37(6), 489–491. doi:10.1002/ab.20407.
Carson, R. C. (1969). Interaction concepts of personality. Perspectives in personality. Chicago: Aldine Publishing Company.
Casto, K. V., & Edwards, D. A. (2016). Testosterone, cortisol, and human competition. Hormones and Behavior, 82, 21–37. doi:10.1016/j.yhbeh.2016.04.004.
Chichinadze, K., Chichinadze, N., Gachechiladze, L., & Lazarashvili, A. (2012). The role of androgens in regulating emotional state and aggressive behavior. Reviews in the Neurosciences, 23(2), 123–133. doi:10.1515/revneuro-2012-0026.
Cicchetti, D., Bronen, R., Spencer, S., Haut, S., Berg, A., Oliver, P., & Tyrer, P. (2006). Rating scales, scales of measurement, issues of reliability: Resolving some critical issues for clinicians and researchers. Journal of Nervous & Mental Disease, 194(8), 557–564. doi:10.1097/01.nmd.0000230392.83607.c5.
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale: Erlbaum.
Dabbs, J. M., Jurkovic, G. J., & Frady, R. L. (1991). Salivary testosterone and cortisol among late adolescent male offenders. Journal of Abnormal Child Psychology, 19(4), 469–478. doi:10.1007/BF00919089.
Dedovic, K., Renwick, R., Mahani, N. K., Engert, V., Lupien, S. J., & Pruessner, J. C. (2005). The Montreal imaging stress task: Using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. Journal of Psychiatry and Neuroscience, 30(5), 319–325.
Denson, T. F., Mehta, P. H., & Ho Tan, D. (2013). Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology, 38(3), 416–424. doi:10.1016/j.psyneuen.2012.07.003.
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130(3), 355–391. doi:10.1037/0033-2909.130.3.355.
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009). Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biological Psychiatry, 65(9), 728–731. doi:10.1016/j.biopsych.2008.10.011.
Edwards, D. A., & Casto, K. V. (2013). Women’s intercollegiate athletic competition: Cortisol, testosterone, and the dual-hormone hypothesis as it relates to status among teammates. Hormones and Behavior, 64(1), 153–160. doi:10.1016/j.yhbeh.2013.03.003.
Evans, K. L., & Hampson, E. (2015). Sex-dependent effects on tasks assessing reinforcement learning and interference inhibition. Frontiers in Psychology, 6(July), 1044. doi:10.3389/fpsyg.2015.01044.
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191.
Finch, W. H., Bolin, J. E., & Kelley, K. (2014). Multilevel Modeling Using R. Boca Raton: CRC Press.
Forbes, E. E., & Dahl, R. E. (2010). Pubertal development and behavior: Hormonal activation of social and motivational tendencies. Brain and Cognition, 72(1), 66–72. doi:10.1016/j.bandc.2009.10.007.
Geniole, S. N., Carré, J. M., & McCormick, C. M. (2011). State, not trait, neuroendocrine function predicts costly reactive aggression in men after social exclusion and inclusion. Biological Psychology, 87(1), 137–145. doi:10.1016/j.biopsycho.2011.02.020.
Heinrichs, M., & Gaab, J. (2007). Neuroendocrine mechanisms of stress and social interaction: Implications for mental disorders. Current Opinion in Psychiatry, 20(2), 158–162. doi:10.1097/YCO.0b013e3280146a13.
Juster, R. P., Raymond, C., Desrochers, A. B., Bourdon, O., Durand, N., Wan, N., et al. (2016). Sex hormones adjust “sex-specific” reactive and diurnal cortisol profiles. Psychoneuroendocrinology, 63, 282–290. doi:10.1016/j.psyneuen.2015.10.012.
Kenny, D. A., & Ledermann, T. (2010). Detecting, measuring, and testing dyadic patterns in the actor-partner interdependence model. Journal of Family Psychology, 24(3), 359–366. doi:10.1037/a0019651.
Kenny, D. A., Kashy, D. A., & Cook, W. L. (2006). Dyadic data analysis. New York: Guilford.
Ketay, S., & Beck, L. A. (2017). Attachment predicts cortisol response and closeness in dyadic social interaction. Psychoneuroendocrinology, 80, 114–121. doi:10.1016/j.psyneuen.2017.03.009.
Kiesler, D. J. (1983). The 1982 interpersonal circle: A taxonomy for complementarity in human transactions. Psychological Review, 90(3), 185–214. doi:10.1037/0033-295X.90.3.185.
Koller, M. (2016a). Package “robustlmm.” Retrieved February 10, 2016, from https://cran.r-project.org/web/packages/robustlmm/robustlmm.pdf.
Koller, M. (2016b). Robustlmm: An R package for robust estimation of linear mixed-effects models. Retrieved February 10, 2016, from https://cran.r-project.org/web/packages/robustlmm/vignettes/rlmer.pdf.
La Marca, R., Waldvogel, P., Thörn, H., Tripod, M., Wirtz, P. H., Pruessner, J. C., & Ehlert, U. (2011). Association between cold face test-induced vagal inhibition and cortisol response to acute stress. Psychophysiology, 48(3), 420–429. doi:10.1111/j.1469-8986.2010.01078.x.
Liening, S. H., Stanton, S. J., Saini, E. K., & Schultheiss, O. C. (2010). Salivary testosterone, cortisol, and progesterone: Two-week stability, interhormone correlations, and effects of time of day, menstrual cycle, and oral contraceptive use on steroid hormone levels. Physiology and Behavior, 99(1), 8–16. doi:10.1016/j.physbeh.2009.10.001.
Locke, K. D. (2011). Circumplex measures of interpersonal constructs. In L. M. Horowitz (Ed.), Handbook of interpersonal psychology : theory, research, assessment, and therapeutic interventions (3rd ed., p. 649). Hoboken : Wiley.
Marceau, K., Ruttle, P. L., Shirtcliff, E. A., Essex, M. J., & Susman, E. J. (2015). Developmental and contextual considerations for adrenal and gonadal hormone functioning during adolescence: Implications for adolescent mental health. Developmental Psychobiology, 57(6), 742–768. doi:10.1002/dev.21214.
McGraw, K. O., & Wong, S. P. (1996). Forming inferences about some intraclass correlations coefficients. Psychological Methods, 1(4), 390–390. doi:10.1037/1082-989X.1.4.390.
Mehta, P. H., & Josephs, R. A. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58(5), 898–906. doi:10.1016/j.yhbeh.2010.08.020.
Mehta, P. H., & Prasad, S. (2015). The dual-hormone hypothesis: A brief review and future research agenda. Current Opinion in Behavioral Sciences, 3, 163–168. doi:10.1016/j.cobeha.2015.04.008.
Mehta, P. H., Wuehrmann, E. V., & Josephs, R. A. (2009). When are low testosterone levels advantageous? The moderating role of individual versus intergroup competition. Hormones and Behavior, 56(1), 158–162. doi:10.1016/j.yhbeh.2009.04.001.
Mehta, P. H., Welker, K. M., Zilioli, S., & Carré, J. M. (2015a). Testosterone and cortisol jointly modulate risk-taking. Psychoneuroendocrinology, 56, 88–99. doi:10.1016/j.psyneuen.2015.02.023.
Mehta, P. H., Mor, S., & Yap, A. J. (2015b). Dual-hormone changes are related to bargaining performance. Psychological Science, 26(9), 1526–1526. doi:10.1177/0956797615602271.
Ponzi, D., Zilioli, S., Mehta, P. H., Maslov, A., & Watson, N. V. (2016). Social network centrality and hormones: The interaction of testosterone and cortisol. Psychoneuroendocrinology, 68(6), 6–13. doi:10.1016/j.psyneuen.2016.02.014.
Popma, A., Vermeiren, R., Geluk, C. A. M. L., Rinne, T., van den Brink, W., Knol, D. L., et al. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61(3), 405–411. doi:10.1016/j.biopsych.2006.06.006.
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31(3), 437–448. doi:10.3102/10769986031004437.
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28(7), 916–931. doi:10.1016/S0306-4530(02)00108-7.
R Core Team. (2016). R: A language and environment for statistical computing. R foundation for statistical computing. Retrieved January 1, 2016, from https://www.r-project.org.
Sadler, P., Ethier, N., Gunn, G. R., Duong, D., & Woody, E. (2009). Are we on the same wavelength? Interpersonal complementarity as shared cyclical patterns during interactions. Journal of Personality and Social Psychology, 97(6), 1005–1020. doi:10.1037/a0016232.
Schultheiss, O. C., Dargel, A., & Rohde, W. (2003). Implicit motives and gonadal steroid hormones: Effects of menstrual cycle phase, oral contraceptive use, and relationship status. Hormones and Behavior, 43(2), 293–301. doi:10.1016/S0018-506X(03)00003-5.
Sherman, G. D., Lerner, J. S., Josephs, R. A., Renshon, J., & Gross, J. J. (2016). The interaction of testosterone and cortisol is associated with attained status in male executives. Journal of Personality and Social Psychology, 110(6), 921–929. doi:10.1037/pspp0000063.
Sollberger, S., Bernauer, T., & Ehlert, U. (2016). Salivary testosterone and cortisol are jointly related to pro-environmental behavior in men. Social Neuroscience, 11(5), 553–566. doi:10.1080/17470919.2015.1117987.
Stephens, M. A. C., Mahon, P. B., McCaul, M. E., & Wand, G. S. (2016). Hypothalamic-pituitary-adrenal axis response to acute psychosocial stress: Effects of biological sex and circulating sex hormones. Psychoneuroendocrinology, 66, 47–55. doi:10.1016/j.psyneuen.2015.12.021.
Stratakis, C. A., & Chrousos, G. P. (1995). Neuroendocrinology and pathophysiology of the stress system. Annals of the New York Academy of Sciences, 771, 1–18. doi:10.1111/j.1749-6632.1995.tb44666.x.
Tackett, J. L., Herzhoff, K., Harden, K. P., Page-Gould, E., & Josephs, R. A. (2014). Personality × hormone interactions in adolescent externalizing psychopathology. Personality Disorders, 5(3), 235–246. doi:10.1037/per0000075.
Tackett, J. L., Reardon, K. W., Herzhoff, K., Page-Gould, E., Harden, K. P., & Josephs, R. A. (2015). Estradiol and cortisol interactions in youth externalizing psychopathology. Psychoneuroendocrinology, 55, 146–153. doi:10.1016/j.psyneuen.2015.02.014.
Turan, B., Tackett, J. L., Lechtreck, M. T., & Browning, W. R. (2015). Coordination of the cortisol and testosterone responses: A dual axis approach to understanding the response to social status threats. Psychoneuroendocrinology, 62, 59–68. doi:10.1016/j.psyneuen.2015.07.166.
Wilcox, R. R. (2010). Fundamentals of modern statistical methods : Substantially improving power and accuracy (2nd ed.). New York: Springer.
Zilioli, S., Ponzi, D., Henry, A., & Maestripieri, D. (2015). Testosterone, cortisol and empathy: Evidence for the dual-hormone hypothesis. Adaptive Human Behavior and Physiology, 1(4), 421–433. doi:10.1007/s40750-014-0017-x.
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We gratefully acknowledge the help of Rita Tatiana Amiel Castro and Serena Fiacco for their helpful comments and English corrections on an earlier draft of this article.
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This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The last author (RL) was supported by a grant of the Swiss National Science Foundation (SNSF) (grant number PBZHP1–133439).
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Lozza, N., Spoerri, C., Ehlert, U. et al. Predicting Social Behavior: Basal and Dynamic Joint Effects of Testosterone and Cortisol. Adaptive Human Behavior and Physiology 3, 255–274 (2017). https://doi.org/10.1007/s40750-017-0069-9
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DOI: https://doi.org/10.1007/s40750-017-0069-9