Human Nature

, Volume 30, Issue 1, pp 98–116 | Cite as

The Influence of Endogenous Opioids on the Relationship between Testosterone and Romantic Bonding

  • Davide PonziEmail author
  • Melissa Dandy


The endogenous opioid system has received attention and extensive research for its effects on reward, pleasure, and pain. However, relative to other neurochemicals, such as oxytocin, vasopressin and dopamine, the function of opioids in regulating human attachment, sociosexuality, and other aspects of human sociality has not received much consideration. For example, nonapeptides (oxytocin and vasopressin) have been extensively studied in animals and humans for their possible roles in mother-offspring attachment, romantic attachment, fatherhood, and social cognition. Likewise, others have proposed models wherein oxytocin and vasopressin are moderators of the relationship between steroid hormones and human social behaviors. Recently, opioids have generated renewed interest in relation to social pain, and importantly, the brain opioid hypothesis of social attachment (BOTSA), which suggests that endogenous opioids are a key implementer in primate and human bonding, has received some support. Here we focus on romantic bonds by proposing that endogenous opioids are an important mechanism mediating reproductive trade-offs through their inhibitory effects on testosterone production.


Opioids Testosterone Mating effort Parenting effort Pair bonding 



The authors would like to thank Drs. Dario Maestripieri and Frederick vom Saal, who kindly reviewed and criticized the manuscript, and we would like to thank two anonymous reviewers for their insightful comments.


  1. Adams, M. L., Sewing, B., Forman, J. B., Meyer, E. R., & Cicero, T. J. (1993). Opioid-induced suppression of rat testicular function. Journal of Pharmacology and Experimental Therapeutics, 266(1), 323–328.Google Scholar
  2. Ali, K., Raphael, J., Khan, S., Labib, M., & Duarte, R. (2016). The effects of opioids on the endocrine system: an overview. Postgraduate Medical Journal, 92(1093), 677–681.CrossRefGoogle Scholar
  3. Alvergne, A., Faurie, C., & Raymond, M. (2009). Variation in testosterone levels and male reproductive effort: insight from a polygynous human population. Hormones and Behavior, 56(5), 491–497.CrossRefGoogle Scholar
  4. Argiolas, A. (1999). Neuropeptides and sexual behaviour. Neuroscience & Biobehavioral Reviews, 23(8), 1127–1142.CrossRefGoogle Scholar
  5. Bales, K. L., del Razo, R. A., Conklin, Q. A., Hartman, S., Mayer, H. S., Rogers, F. D., ... & Witczak, L. R. (2017). Titi monkeys as a novel non-human primate model for the neurobiology of pair bonding. The Yale Journal of Biology and Medicine, 90(3), 373–387.Google Scholar
  6. Bancroft, J. (2005). The endocrinology of sexual arousal. Journal of Endocrinology, 186(3), 411–427.CrossRefGoogle Scholar
  7. Barr, C., Schwwandt, M., Lindell, S., Higley, J., Maestripieri, D., Goldman, D., Suomi, S., & Heilig, M. (2008). Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proceedings of the National Academy of Sciences, 105(13), 5277–5281.CrossRefGoogle Scholar
  8. Blanc, A. K., & Rutenberg, N. (1991). Coitus and contraception: the utility of data on sexual intercourse for family planning programs. Studies in Family Planning, 22(3), 162–176.CrossRefGoogle Scholar
  9. Bond, C., LaForge, K. S., Tian, M., Melia, D., Zhang, S., Borg, L., ... & Tischfield, J. A. (1998). Single-nucleotide polymorphism in the human mu opioid receptor gene alters β-endorphin binding and activity: possible implications for opiate addiction. Proceedings of the National Academy of Sciences, 95(16), 9608–9613.Google Scholar
  10. Bowlby, J. (1988). A secure base: Parent-child attachment and healthy human development. New York: Basic Books.Google Scholar
  11. Burnham, T. C., Chapman, J. F., Gray, P. B., McIntyre, M. H., Lipson, S. F., & Ellison, P. T. (2003). Men in committed, romantic relationships have lower testosterone. Hormones and Behavior, 44(2), 119–122.CrossRefGoogle Scholar
  12. Carré, J. M., Putnam, S. K., & McCormick, C. M. (2009). Testosterone responses to competition predict future aggressive behavior at a cost to reward in men. Psychoneuroendocrinology, 34, 561–570.CrossRefGoogle Scholar
  13. Carter, C. S. (2014). Oxytocin pathways and the evolution of human behavior. Annual Review of Psychology, 65, 17–39.CrossRefGoogle Scholar
  14. Carter, C. S., & Keverne, E. B. (2002). The neurobiology of social affiliation and pair bonding. In D. W. Pfaff et al. (Eds.) Hormones, brain and behavior (pp. 299–337). San Diego: Elsevier.Google Scholar
  15. Chapais, B. (2013). Monogamy, strongly bonded groups, and the evolution of human social structure. Evolutionary Anthropology, 22(2), 52–65.CrossRefGoogle Scholar
  16. Cicero, T., Schainker, B., & Meyer, E. (1979). Endogenous opioids participate in the regulation of the hypothalamic-pituitary-luteinizing hormone axis and testosterone’s negative feedback control of luteinizing hormone. Endocrinology, 104(5), 1286–1291.CrossRefGoogle Scholar
  17. Cohen, E. E., Ejsmond-Frey, R., Knight, N., & Dunbar, R. I. (2010). Rowers' high: behavioural synchrony is correlated with elevated pain thresholds. Biology Letters, 6(1), 106–108.CrossRefGoogle Scholar
  18. Daniell, H. W. (2002). Hypogonadism in men consuming sustained-action oral opioids. The Journal of Pain, 3(5), 377–384.CrossRefGoogle Scholar
  19. Del Giudice, M. (2009). Sex, attachment, and the development of reproductive strategies. Behavioral and Brain Sciences, 32(1), 1–21.CrossRefGoogle Scholar
  20. Delitala, G., Grossman, A., & Besser, M. (1983a). Differential effects of opiate peptides and alkaloids on anterior pituitary hormone secretion. Neuroendocrinology, 37(4), 275–279.CrossRefGoogle Scholar
  21. Delitala, G., Grossman, A., & Besser, G. M. (1983b). The participation of hypothalamic dopamine in morphine-induced prolactin release in man. Clinical Endocrinology, 19(4), 437–444.CrossRefGoogle Scholar
  22. Donaldson, Z., & Young, L. (2016). The neurobiology of genetics and affiliation and social bonding in animal models. In J. C. Gewirtz & Y.-K. Kim (Eds.), Animal models of behavior genetics (pp. 101–134). New York: Springer.CrossRefGoogle Scholar
  23. Dornan, W. A., & Malsbury, C. W. (1989). Neuropeptides and male sexual behavior. Neuroscience & Biobehavioral Reviews, 13(1), 1–15.CrossRefGoogle Scholar
  24. Dunbar, R. I. M. (2010). The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. Neuroscience & Biobehavioral Reviews, 34(2), 260–268.CrossRefGoogle Scholar
  25. Dunbar, R. I. M., Baron, R., Frangou, A., Pearce, E., van Leeuwin, E. J., Stow, J., ... & Van Vugt, M. (2011). Social laughter is correlated with an elevated pain threshold. Proceedings of the Royal Society of London B: Biological Sciences, rspb20111373.Google Scholar
  26. Edelstein, R., Chopik, W., & Kean, E. (2011). Sociosexuality moderates the association between testosterone and relationship status in men and women. Hormones and Behavior, 60, 248–255.CrossRefGoogle Scholar
  27. Fabbri, A., Jannini, E. A., Gnessi, L., Ulisse, S., Moretti, C., & Isidori, A. (1989). Neuroendocrine control of male reproductive function. The opioid system as a model of control at multiple sites. Journal of Steroid Biochemistry, 32(1), 145–150.CrossRefGoogle Scholar
  28. Feldman, R. (2017). The neurobiology of human attachments. Trends in Cognitive Sciences, 21(2), 80–99.CrossRefGoogle Scholar
  29. Ferin, M. (1984). Endogenous opioid peptides and the menstrual cycle. Trends in Neurosciences, 7(6), 194–196.CrossRefGoogle Scholar
  30. Ferin, M. (1999). Stress and the reproductive cycle. Journal of Clinical Endocrinology & Metabolism, 84(6), 1768–1774.CrossRefGoogle Scholar
  31. Fleming, A. S., Corter, C., Stallings, J., & Steiner, M. (2002). Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Hormones and Behavior, 42(4), 399–413.CrossRefGoogle Scholar
  32. Fletcher, G. J., Simpson, J. A., Campbell, L., & Overall, N. C. (2015). Pair-bonding, romantic love, and evolution: the curious case of Homo sapiens. Perspectives on Psychological Science, 10(1), 20–36.CrossRefGoogle Scholar
  33. Flinn, M. V., Quinlan, R. J., Ward, C. V., & Coe, M. K. (2007). Evolution of the human family: cooperative males, long social childhoods, smart mothers, and extended kin networks. Family Relationships, 16–38.Google Scholar
  34. Flinn, M. V., Ponzi, D., & Muehlenbein, M. P. (2012). Hormonal mechanisms for regulation of aggression in human coalitions. Human Nature, 23(1), 68–88.CrossRefGoogle Scholar
  35. Geary, D. C. (2000). Evolution and proximate expression of human paternal investment. Psychological Bulletin, 126(1), 55–77.CrossRefGoogle Scholar
  36. Gettler, L. T., & Oka, R. C. (2016). Aging US males with multiple sources of emotional social support have low testosterone. Hormones and Behavior, 78, 32–42.CrossRefGoogle Scholar
  37. Gettler, L., McDade, T., Feranil, A., & Kuzawa, C. (2011a). Longitudinal evidence that fatherhood decreases testosterone in human males. Proceedings of the National Academy of Sciences, 108(39), 16194–16199.CrossRefGoogle Scholar
  38. Gettler, L. T., Mcdade, T. W., & Kuzawa, C. W. (2011b). Cortisol and testosterone in Filipino young adult men: evidence for co-regulation of both hormones by fatherhood and relationship status. American Journal of Human Biology, 23(5), 609–620.CrossRefGoogle Scholar
  39. Gettler, L. T., McDade, T. W., Feranil, A. B., & Kuzawa, C. W. (2012a). Prolactin, fatherhood, and reproductive behavior in human males. American Journal of Physical Anthropology, 148(3), 362–370.CrossRefGoogle Scholar
  40. Gettler, L. T., McKenna, J. J., McDade, T. W., Agustin, S. S., & Kuzawa, C. W. (2012b). Does cosleeping contribute to lower testosterone levels in fathers? Evidence from the Philippines. PLoS One, 7(9), e41559.CrossRefGoogle Scholar
  41. Gettler, L. T., McDade, T. W., Agustin, S. S., Feranil, A. B., & Kuzawa, C. W. (2013). Do testosterone declines during the transition to marriage and fatherhood relate to men's sexual behavior? Evidence from the Philippines. Hormones and Behavior, 64(5), 755–763.CrossRefGoogle Scholar
  42. Gettler, L. T., Ryan, C. P., Eisenberg, D. T., Rzhetskaya, M., Hayes, M. G., Feranil, A. B., ... & Kuzawa, C. W. (2017). The role of testosterone in coordinating male life history strategies: the moderating effects of the androgen receptor CAG repeat polymorphism. Hormones and Behavior, 87, 164–175.Google Scholar
  43. Gilbeau, P. M., & Smith, C. G. (1985). Naloxone reversal of stress-induced reproductive effects in the male rhesus monkey. Neuropeptides, 5(4–6), 335–338.CrossRefGoogle Scholar
  44. Gilbeau, P. M., Almirez, R. G., Holaday, J. W., & Smith, C. G. (1985). Opioid effects on plasma concentrations of luteinizing hormone and prolactin in the adult male rhesus monkey. Journal of Clinical Endocrinology & Metabolism, 60(2), 299–305.CrossRefGoogle Scholar
  45. Goodson, J. L. (2013). Deconstructing sociality, social evolution and relevant nonapeptide functions. Psychoneuroendocrinology, 38(4), 465–478.CrossRefGoogle Scholar
  46. Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010). Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Hormones and Behavior, 58(3), 513–518.CrossRefGoogle Scholar
  47. Graves, F. C. K., Wallen, K., & Maestripieri, D. (2002). Opioids and attachment in rhesus macaque abusive mothers. Behavioral Neuroscience, 116, 489–493.CrossRefGoogle Scholar
  48. Gray, P. B. (2003). Marriage, parenting, and testosterone variation among Kenyan Swahili men. American Journal of Physical Anthropology, 122(3), 279–286.CrossRefGoogle Scholar
  49. Gray, P. B., & Garcia, J. R. (2013). Evolution and human sexual behavior. Cambridge: Harvard University Press.Google Scholar
  50. Gray, P. B., Kahlenberg, S. M., Barrett, E. S., Lipson, S. F., & Ellison, P. T. (2002). Marriage and fatherhood are associated with lower testosterone in males. Evolution and Human Behavior, 23(3), 193–201.CrossRefGoogle Scholar
  51. Gray, P. B., Campbell, B. C., Marlowe, F. W., Lipson, S. F., & Ellison, P. T. (2004). Social variables predict between-subject but not day-to-day variation in the testosterone of US men. Psychoneuroendocrinology, 29(9), 1153–1162.CrossRefGoogle Scholar
  52. Gray, P. B., Yang, C. F. J., & Pope, H. G. (2006). Fathers have lower salivary testosterone levels than unmarried men and married non-fathers in Beijing, China. Proceedings of the Royal Society of London B: Biological Sciences, 273(1584), 333–339.CrossRefGoogle Scholar
  53. Gray, P. B., Ellison, P. T., & Campbell, B. C. (2007). Testosterone and marriage among Ariaal men of northern Kenya. Current Anthropology, 48(5), 750–755.CrossRefGoogle Scholar
  54. Hadden, B., Smith, V., & Webster, G. (2013). Relationship duration moderates associations between attachment and relationship quality: meta-analytic support for the temporal adult romantic attachment model. Personality and Social Psychology Review, 1–17.Google Scholar
  55. Herbert, J. (1993). Peptides in the limbic system: neurochemical codes for coordinated adaptive responses to behavioural and physiological demand. Progress in Neurobiology, 41(6), 723–791.CrossRefGoogle Scholar
  56. Higham, J. P., Barr, C. S., Hoffman, C. L., Mandalaywala, T. M., Parker, K. J., & Maestripieri, D. (2011). Mu-opioid receptor (OPRM1) variation, oxytocin levels, and maternal attachment in free-ranging rhesus macaques. Behavioral Neuroscience, 152, 131–136.CrossRefGoogle Scholar
  57. Holmboe, S. A., Priskorn, L., Jørgensen, N., Skakkebaek, N. E., Linneberg, A., Juul, A., & Andersson, A. M. (2017). Influence of marital status on testosterone levels — a ten-year follow-up of 1113 men. Psychoneuroendocrinology, 80, 155–161.CrossRefGoogle Scholar
  58. Inagaki, T. K., Ray, L. A., Irwin, M. R., Way, B. M., & Eisenberger, N. I. (2016). Opioids and social bonding: naltrexone reduces feelings of social connection. Social Cognitive and Affective Neuroscience, 11(5), 728–735.CrossRefGoogle Scholar
  59. Jasienska, G., Jasienski, M., & Ellison, P. T. (2012). Testosterone levels correlate with the number of children in human males, but the direction of the relationship depends on paternal education. Evolution and Human Behavior, 33(6), 665–671.CrossRefGoogle Scholar
  60. Johnson, K. V. A., & Dunbar, R. I. (2016). Pain tolerance predicts human social network size. Scientific Reports, 6, 25267.CrossRefGoogle Scholar
  61. Kalin, N. H., Shelton, S. E., & Barksdale, C. M. (1988). Opiate modulation of separation-induced distress in non-human primates. Brain Research, 440(2), 285–292.CrossRefGoogle Scholar
  62. Kalin, N. H., Shelton, S. E., & Lynn, D. E. (1995). Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology, 20(7), 735–742.CrossRefGoogle Scholar
  63. Keverne, E. B., Martensz, N. D., & Tuite, B. (1989). Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology, 14(1–2), 155–161.CrossRefGoogle Scholar
  64. Kirkpatrick, L. A. (1998). Evolution, pair-bonding, and reproductive strategies: A reconceptualization of adult attachment. In J. A. Simpson & W. S. Rholes (Eds.), Attachment theory and close relationships (pp. 353–393). New York: Guilford Press.Google Scholar
  65. Koepp, M. J., Hammers, A., Lawrence, A. D., Asselin, M. C., Grasby, P. M., & Bench, C. J. (2009). Evidence for endogenous opioid release in the amygdala during positive emotion. Neuroimage, 44(1), 252–256.CrossRefGoogle Scholar
  66. Kuzawa, C. W., Gettler, L. T., Muller, M. N., McDade, T. W., & Feranil, A. B. (2009). Fatherhood, pair-bonding and testosterone in the Philippines. Hormones and Behavior, 56(4), 429–435.CrossRefGoogle Scholar
  67. Kuzawa, C. W., Gettler, L. T., Huang, Y. Y., & McDade, T. W. (2010). Mothers have lower testosterone than non-mothers: Evidence from the Philippines. Hormones and Behavior, 57(4–5), 441–447.CrossRefGoogle Scholar
  68. Lafisca, S., Bolelli, G., Franceschetti, F., Danieli, A., Tagliaro, F., Marigo, M., & Flamigni, C. (1985). Free and bound testosterone in male heroin addicts. In Chambers et al. (Eds.) Receptors and other targets for toxic substances (pp. 394–397). Berlin: Springer.Google Scholar
  69. Landau, R., Kern, C., Columb, M. O., Smiley, R. M., & Blouin, J. L. (2008). Genetic variability of the μ-opioid receptor influences intrathecal fentanyl analgesia requirements in laboring women. Pain, 139(1), 5–14.CrossRefGoogle Scholar
  70. Le Merrer, J., Becker, J. A., Befort, K., & Kieffer, B. L. (2009). Reward processing by the opioid system in the brain. Physiological Reviews, 89(4), 1379–1412.CrossRefGoogle Scholar
  71. Loseth, G. E., Ellingsen, D. M., & Leknes, S. (2014). State-dependent μ-opioid modulation of social motivation—a model. Frontiers in Behavioral Neuroscience, 8, 430.CrossRefGoogle Scholar
  72. Machin, A. J., & Dunbar, R. I. (2011). The brain opioid theory of social attachment: a review of the evidence. Behaviour, 148(9–10), 985–1025.CrossRefGoogle Scholar
  73. Maestripieri, D., Klimczuk, A., Traficonte, D., & Wilson, M. C. (2014). Ethnicity-related variation in sexual promiscuity, relationship status, and testosterone levels in men. Evolutionary Behavioral Sciences, 8(2), 96–101.CrossRefGoogle Scholar
  74. Mague, S. D., Isiegas, C., Huang, P., Liu-Chen, L. Y., Lerman, C., & Blendy, J. A. (2009). Mouse model of OPRM1 (A118G) polymorphism has sex-specific effects on drug-mediated behavior. Proceedings of the National Academy of Sciences, 106(26), 10847–10852.CrossRefGoogle Scholar
  75. Manninen, S., Tuominen, L., Dunbar, R. I., Karjalainen, T., Hirvonen, J., Arponen, E., Hari, R., Jääskeläinen, I. P., Sams, M., & Nummenmaa, L. (2017). Social laughter triggers endogenous opioid release in humans. Journal of Neuroscience, 37(25), 6125–6131.CrossRefGoogle Scholar
  76. Martel, F. L., Nevison, C. M., Rayment, F. D., Simpson, M. J., & Keverne, E. B. (1993). Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology, 18(4), 307–321.CrossRefGoogle Scholar
  77. Martel, F. L., Nevison, C. M., Simpson, M. J., & Keverne, E. B. (1995). Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Developmental Psychobiology, 28(2), 71–84.CrossRefGoogle Scholar
  78. Martensz, N. D., Vellucci, S. V., Keverne, E. B., & Herbert, J. (1986). β-Endorphin levels in the cerebrospinal fluid of male talapoin monkeys in social groups related to dominance status and the luteinizing hormone response to naloxone. Neuroscience, 18(3), 651–658.CrossRefGoogle Scholar
  79. Master, S. L., Eisenberger, N. I., Taylor, S. E., Naliboff, B. D., Shirinyan, D., & Lieberman, M. D. (2009). A picture's worth: partner photographs reduce experimentally induced pain. Psychological Science, 20(11), 1316–1318.CrossRefGoogle Scholar
  80. McGuire, M., & Troisi, A. (1998). Darwinian psychiatry. Oxford: Oxford University Press.CrossRefGoogle Scholar
  81. McIntyre, M., Gangestad, S. W., Gray, P. B., Chapman, J. F., Burnham, T. C., O'rourke, M. T., & Thornhill, R. (2006). Romantic involvement often reduces men's testosterone levels—but not always: the moderating role of extrapair sexual interest. Journal of Personality and Social Psychology, 91(4), 642–651.CrossRefGoogle Scholar
  82. McNulty, J. K., Wenner, C. A., & Fisher, T. D. (2016). Longitudinal associations among relationship satisfaction, sexual satisfaction, and frequency of sex in early marriage. Archives of Sexual Behavior, 45(1), 85–97.CrossRefGoogle Scholar
  83. Misiti, A., Turillazzi, P. G., Zapponi, G. A., & Loizzo, A. (1991). Heroin induces changes in mother-infant monkey communication and subsequent disruption of their dyadic interaction. Pharmacological Research, 24, 93–104.CrossRefGoogle Scholar
  84. Muller, M. N. (2017). Testosterone and reproductive effort in male primates. Hormones and Behavior, 91, 36–51.CrossRefGoogle Scholar
  85. Muller, M. N., & Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: a test of the “challenge hypothesis”. Animal Behaviour, 67(1), 113–123.CrossRefGoogle Scholar
  86. Muller, M. N., Marlowe, F. W., Bugumba, R., & Ellison, P. T. (2009). Testosterone and paternal care in East African foragers and pastoralists. Proceedings of the Royal Society of London B: Biological Sciences, 276(1655), 347–354.CrossRefGoogle Scholar
  87. Nelson, R. J. (2011). An introduction to behavioral endocrinology. Sunderland: Sinauer Associates.Google Scholar
  88. Nelson, E. E., & Panksepp, J. (1998). Brain substrates of infant–mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neuroscience & Biobehavioral Reviews, 22(3), 437–452.CrossRefGoogle Scholar
  89. Nummenmaa, L., Manninen, S., Tuominen, L., Hirvonen, J., Kalliokoski, K., Nuutila, P., Jääskeläinen, I., Hara, R., Dunbar, R., & Sams, M. (2015). Adult attachment style is associated with cerebral μ-opioid receptor availability in humans. Human Brain Mapping, 36(9), 3621–3628.CrossRefGoogle Scholar
  90. Oxford, J., Ponzi, D., & Geary, D. C. (2010). Hormonal responses differ when playing violent video games against an ingroup and outgroup. Evolution and Human Behavior, 31(3), 201–209.CrossRefGoogle Scholar
  91. Panksepp, J., Herman, B., Vilberg, T., Bishop, P., & DeEskinazi, F. (1980). Endogenous opioids and social behavior. Neuroscience & Biobehavioral Review, 4, 473–487.CrossRefGoogle Scholar
  92. Panksepp, J., Nelson, E., & Siviy, S. (1994). Brain opioids and mother-infant social motivation. Acta Paediatrica, 83(Suppl. 397), 40–46.CrossRefGoogle Scholar
  93. Pearce, E., Wlodarski, R., Machin, A., & Dunbar, R. I. (2017). Variation in the β-endorphin, oxytocin, and dopamine receptor genes is associated with different dimensions of human sociality. Proceedings of the National Academy of Sciences, 201700712.Google Scholar
  94. Peciña, M., Love, T., Stohler, C. S., Goldman, D., & Zubieta, J. K. (2015). Effects of the Mu opioid receptor polymorphism (OPRM1 A118G) on pain regulation, placebo effects and associated personality trait measures. Neuropsychopharmacology, 40(4), 957–965.Google Scholar
  95. Pende, A., Musso, N. R., Montaldi, M. L., Pastorino, G., Arzese, M., & Devilla, L. (1986). Evaluation of the effects induced by four opiate drugs, with different affinities to opioid receptor subtypes, on anterior pituitary LH, TSH, PRL and GH secretion and on cortisol secretion in normal men. Biomedicine & Pharmacotherapy/Biomedecine & Pharmacotherapie, 40(5), 178–182.Google Scholar
  96. Pfaus, J. G. (2009). Reviews: pathways of sexual desire. The Journal of Sexual Medicine, 6(6), 1506–1533.CrossRefGoogle Scholar
  97. Pfaus, J. G., & Gorzalka, B. B. (1987). Opioids and sexual behavior. Neuroscience and Biobehavioral Reviews, 11(1), 1–34.CrossRefGoogle Scholar
  98. Pollet, T. V., van der Meij, L., Cobey, K. D., & Buunk, A. P. (2011). Testosterone levels and their associations with lifetime number of opposite sex partners and remarriage in a large sample of American elderly men and women. Hormones and Behavior, 60(1), 72–77.CrossRefGoogle Scholar
  99. Roberts, L. J., Finch, P. M., Pullan, P. T., Bhagat, C. I., & Price, L. M. (2002). Sex hormone suppression by intrathecal opioids: a prospective study. Clinical Journal of Pain, 18(3), 144–148.CrossRefGoogle Scholar
  100. Robles, T. F., & Kiecolt-Glaser, J. K. (2003). The physiology of marriage: pathways to health. Physiology & Behavior, 79(3), 409–416.CrossRefGoogle Scholar
  101. Roney, J., & Gettler, L. (2015). The role of testosterone in human romantic relationships. Current Opinion in Psychology, 1, 81–86.CrossRefGoogle Scholar
  102. Roney, J. R., & Simmons, Z. L. (2013). Hormonal predictors of sexual motivation in natural menstrual cycles. Hormones and Behavior, 63(4), 636–645.CrossRefGoogle Scholar
  103. Saltzman, W., & Ziegler, T. E. (2014). Functional significance of hormonal changes in mammalian fathers. Journal of Neuroendocrinology, 26(10), 685–696.CrossRefGoogle Scholar
  104. Sapolsky, R. M., & Krey, L. C. (1988). Stress-induced suppression of luteinizing hormone concentrations in wild baboons: role of opiates. The Journal of Clinical Endocrinology & Metabolism, 66(4), 722–726.CrossRefGoogle Scholar
  105. Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1), 55–89.Google Scholar
  106. Scheele, D., Striepens, N., Güntürkün, O., Deutschländer, S., Maier, W., Kendrick, K. M., & Hurlemann, R. (2012). Oxytocin modulates social distance between males and females. Journal of Neuroscience, 32(46), 16074–16079.CrossRefGoogle Scholar
  107. Schindler, A., Thomasius, R., Petersen, K., & Sack, P. M. (2009). Heroin as an attachment substitute? Differences in attachment representations between opioid, ecstasy and cannabis abusers. Attachment & Human Development, 11(3), 307–330.CrossRefGoogle Scholar
  108. Schino, G., & Troisi, A. (1992). Opiate receptor blockade in juvenile macaques: effect on affiliative interactions with their mothers and group companions. Brain Research, 576(1), 125–130.CrossRefGoogle Scholar
  109. Schneiderman, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2012). Oxytocin during the initial stages of romantic attachment: relations to couples’ interactive reciprocity. Psychoneuroendocrinology, 37(8), 1277–1285.CrossRefGoogle Scholar
  110. Schneiderman, I., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2014). Mutual influences between partners’ hormones shape conflict dialog and relationship duration at the initiation of romantic love. Social Neuroscience, 9(4), 337–351.CrossRefGoogle Scholar
  111. Shayit, M., Nowak, R., Keller, M., & Weller, A. (2003). Establishment of a preference by the newborn lamb for its mother: the role of opioids. Behavioral Neuroscience, 117(3), 446–454.CrossRefGoogle Scholar
  112. Sia, A. T., Lim, Y., Lim, E. C., Goh, R. W., Law, H. Y., Landau, R., ... & Tan, E. C. (2008). A118G single nucleotide polymorphism of human μ-opioid receptor gene influences pain perception and patient-controlled intravenous morphine consumption after intrathecal morphine for postcesarean analgesia. Anesthesiology, 109(3), 520–526.Google Scholar
  113. Sobolewski, M. E., Brown, J. L., & Mitani, J. C. (2013). Female parity, male aggression, and the challenge hypothesis in wild chimpanzees. Primates, 54(1), 81–88.CrossRefGoogle Scholar
  114. Storey, A. E., & Ziegler, T. E. (2016). Primate paternal care: interactions between biology and social experience. Hormones and Behavior, 77, 260–271.CrossRefGoogle Scholar
  115. Storey, A. E., Walsh, C. J., Quinton, R. L., & Wynne-Edwards, K. E. (2000). Hormonal correlates of paternal responsiveness in new and expectant fathers. Evolution and Human Behavior, 21(2), 79–95.CrossRefGoogle Scholar
  116. Stubbs, W. A., Jones, A., Edwards, C. R. W., Delitala, G., Jeffcoate, W. J., Ratter, S. J., Besser, G. M., Bloom, S. R., & Alberti, K. G. M. M. (1978). Hormonal and metabolic responses to an enkephalin analogue in normal man. The Lancet, 312(8102), 1225–1227.CrossRefGoogle Scholar
  117. Tarr, B., Launay, J., Cohen, E., & Dunbar, R. (2015). Synchrony and exertion during dance independently raise pain threshold and encourage social bonding. Biology Letters, 11(10), 20150767.CrossRefGoogle Scholar
  118. Tarr, B., Launay, J., Benson, C., & Dunbar, R. I. (2017). Naltrexone blocks endorphins released when dancing in synchrony. Adaptive Human Behavior and Physiology, 3(3), 241–254.CrossRefGoogle Scholar
  119. Troisi, A., Frazzetto, G., Carola, V., Di Lorenzo, G., Coviello, M., D’Amato, F., Moles, A., Siracusano, A., & Gross, C. (2011a). Social hedonic capacity is associated with the A118G polymorphism of the mu-opioid receptor gene (OPRM1) in adult healthy volunteers and psychiatric patients. Social Neuroscience, 6(1), 88–97.CrossRefGoogle Scholar
  120. Troisi, A., Frazzetto, G., Carola, V., Di Lorenzo, G., Coviello, M., Siracusano, A., & Gross, C. (2011b). Variation in the μ-opioid receptor gene (OPRM1) moderates the influence of early maternal care on fearful attachment. Social Cognitive and Affective Neuroscience, 7(5), 542–547.CrossRefGoogle Scholar
  121. Ulmer-Yaniv, A., Avitsur, R., Kanat-Maymon, Y., Schneiderman, I., Zagoory-Sharon, O., & Feldman, R. (2016). Affiliation, reward, and immune biomarkers coalesce to support social synchrony during periods of bond formation in humans. Brain, Behavior, and Immunity, 56, 130–139.CrossRefGoogle Scholar
  122. van Anders, S., & Goldey, K. (2010). Testosterone and partnering are linked via relationship status for women and ‘relationship orientation’ for men. Hormones and Behavior, 58, 820–826.CrossRefGoogle Scholar
  123. van Anders, S. M., & Watson, N. V. (2007). Testosterone levels in women and men who are single, in long-distance relationships, or same-city relationships. Hormones and Behavior, 51(2), 286–291.CrossRefGoogle Scholar
  124. van Anders, S. M., Hamilton, L. D., & Watson, N. V. (2007). Multiple partners are associated with higher testosterone in North American men and women. Hormones and Behavior, 51(3), 454–459.CrossRefGoogle Scholar
  125. van Anders, S. M., Goldey, K. L., & Kuo, P. X. (2011). The steroid/peptide theory of social bonds: integrating testosterone and peptide responses for classifying social behavioral contexts. Psychoneuroendocrinology, 36(9), 1265–1275.CrossRefGoogle Scholar
  126. van Furth, W. R., Wolterink, G., & van Ree, J. M. (1995). Regulation of masculine sexual behavior: involvement of brain opioids and dopamine. Brain Research Reviews, 21(2), 162–184.CrossRefGoogle Scholar
  127. Veldhuis, J. D., Rogol, A. D., Samojlik, E., & Ertel, N. H. (1984). Role of endogenous opiates in the expression of negative feedback actions of androgen and estrogen on pulsatile properties of luteinizing hormone secretion in man. Journal of Clinical Investigation, 74(1), 47–55.CrossRefGoogle Scholar
  128. Vuong, C., Van Uum, S. H., O'dell, L. E., Lutfy, K., & Friedman, T. C. (2009). The effects of opioids and opioid analogs on animal and human endocrine systems. Endocrine Reviews, 31(1), 98–132.CrossRefGoogle Scholar
  129. Way, B. M., Taylor, S. E., & Eisenberger, N. I. (2009). Variation in the μ-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proceedings of the National Academy of Sciences, 106(35), 15079–15084.CrossRefGoogle Scholar
  130. Weinstein, D., Launay, J., Pearce, E., Dunbar, R. I., & Stewart, L. (2016). Group music performance causes elevated pain thresholds and social bonding in small and large groups of singers. Evolution and Human Behavior, 37(2), 152–158.CrossRefGoogle Scholar
  131. Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2014). Oxytocin administration, salivary testosterone, and father–infant social behavior. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 49, 47–52.CrossRefGoogle Scholar
  132. Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology, 15(8), 711–724.CrossRefGoogle Scholar
  133. Wingfield, J. C., Hegner, R. E., Dufty Jr., A. M., & Ball, G. F. (1990). The" challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. The American Naturalist, 136(6), 829–846.CrossRefGoogle Scholar
  134. Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M., & Richardson, R. D. (1998). Ecological bases of hormone-behavior interactions: the “emergency life history stage.” American Zoologist, 38(1), 191–206.CrossRefGoogle Scholar
  135. Winking, J., Gurven, M., & Kaplan, H. (2011). The impact of parents and self-selection on child survival among the Tsimane of Bolivia. Current Anthropology, 52(2), 277–284.CrossRefGoogle Scholar
  136. Wynne-Edwards, K. E. (2001). Hormonal changes in mammalian fathers. Hormones and Behavior, 40(2), 139–145.CrossRefGoogle Scholar
  137. Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011). The neurobiology of pair bonding: insights from a socially monogamous rodent. Frontiers in Neuroendocrinology, 32(1), 53–69.CrossRefGoogle Scholar
  138. Zhang, Y., Wang, D., Johnson, A. D., Papp, A. C., & Sadée, W. (2005). Allelic expression imbalance of human mu opioid receptor (OPRM1) caused by variant A118G. Journal of Biological Chemistry, 280(38), 32618–32624.CrossRefGoogle Scholar
  139. Ziegler, T. E., & Crockford, C. (2017). Neuroendocrine control in social relationships in non-human primates: field-based evidence. Hormones and Behavior, 91, 107–121.CrossRefGoogle Scholar
  140. Zilioli, S., Ponzi, D., Henry, A., Kubicki, K., Nickels, N., Wilson, M. C., & Maestripieri, D. (2016). Interest in babies negatively predicts testosterone responses to sexual visual stimuli among heterosexual young men. Psychological Science, 27(1), 114–118.CrossRefGoogle Scholar
  141. Zubieta, J. K., Ketter, T. A., Bueller, J. A., Xu, Y., Kilbourn, M. R., Young, E. A., & Koeppe, R. A. (2003). Regulation of human affective responses by anterior cingulate and limbic μ-opioid neurotransmission. Archives of General Psychiatry, 60(11), 1145–1153.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of PsychologyOklahoma State UniversityStillwaterUSA

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