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Endocrinology of Human Female Sexuality, Mating, and Reproductive Behavior

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Endocrinology of Human Female Sexuality, Mating, and Reproductive Behavior Hormones and Behavior 91 (2017) 19–35 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh Review article Endocrinology of human female sexuality, mating, and reproductive behavior Natalie V. Motta-Mena a, David A. Puts b,⁎ a Department of Psychology, Pennsylvania State University, University Park, PA 16802, United States b Department of Anthropology, Center for Brain, Behavior, and Cognition, Center for Human Evolution and Diversity, Pennsylvania State University, University Park, PA 16802¸ United States article info abstract Article history: Hormones orchestrate and coordinate human female sexual development, sexuality, and reproduction in relation Received 14 March 2016 to three types of phenotypic changes: life history transitions such as puberty and childbirth, responses to contex- Revised 2 November 2016 tual factors such as caloric intake and stress, and cyclical patterns such as the ovulatory cycle. Here, we review the Accepted 12 November 2016 endocrinology underlying women's reproductive phenotypes, including sexual orientation and gender identity, Available online 17 November 2016 mate preferences, competition for mates, sex drive, and maternal behavior. We highlight distinctive aspects of Keywords: women's sexuality such as the possession of sexual ornaments, relatively cryptic fertile windows, extended sex- — Cortisol ual behavior across the ovulatory cycle, and a period of midlife reproductive senescence and we focus on how Estradiol hormonal mechanisms were shaped by selection to produce adaptive outcomes. We conclude with suggestions Ovarian hormones for future research to elucidate how hormonal mechanisms subserve women's reproductive phenotypes. Oxytocin, progesterone © 2016 Elsevier Inc. All rights reserved. Prolactin Sexuality Testosterone Contents 1. Introduction............................................................... 20 2. Earlydevelopment:sexualorientationandgenderidentity.......................................... 20 3. Puberty................................................................. 22 4. Matingcompetition............................................................ 23 4.1. Sexualornaments......................................................... 23 4.2. Cuestoovulatoryphase...................................................... 24 4.3. Intrasexualcompetition....................................................... 24 5. Sexdriveandsociosexuality........................................................ 25 5.1. Intercoursefrequency....................................................... 25 5.2. Sexdrive............................................................. 25 5.3. Sociosexuality........................................................... 26 6. Matepreferences............................................................. 26 6.1. Ovulatorycycleshifts........................................................ 26 6.2. Femaleorgasm.......................................................... 27 7. Motherhood............................................................... 27 8. Menopause............................................................... 28 9. Discussion................................................................ 29 Acknowledgments............................................................... 29 AppendixA. Supplementarydata....................................................... 29 References.................................................................. 29 ⁎ Corresponding author at: Department of Anthropology, 408 Carpenter Building, Pennsylvania State University, University Park, PA 16802, United States. E-mail address: [email protected] (D.A. Puts). http://dx.doi.org/10.1016/j.yhbeh.2016.11.012 0018-506X/© 2016 Elsevier Inc. All rights reserved. 20 N.V. Motta-Mena, D.A. Puts / Hormones and Behavior 91 (2017) 19–35 1. Introduction effects depend on the stage of development, as well. Hormones also ad- just resource allocation to mating and reproduction in response to con- In some ways, women are typical female primates. In the broad arc textual factors, such as caloric availability, psychosocial stress, and of their lifespans, women reproduce at modest rates and engage in ex- physical challenge. Finally, hormones exhibit cyclical fluctuations, tensive parental investment—that is, they have a primate's characteris- which adjust behavior and physiology according to sleep-wake cycles tically slow life history (Jones, 2011). As in many other primates, and the ovulatory cycle. humans also form complex social groups and evince sexually differenti- In the current manuscript, we review evidence regarding how hor- ated behaviors both during development and in adulthood (Wallen, mones orchestrate, coordinate, and regulate key components of 2005). Some of the earliest developing and most sexually differentiated human female sexual development, life history, and reproductive strat- components of human psychology are gender identity, which directs egies, as well as how behaviors and the environment feed back onto gendered socialization and behavior, and sexual orientation. Following hormone production. We focus on how these relationships were shaped puberty, the process of sexual maturation, women mate and gestate, by selection to produce adaptive outcomes. Sections are ordered nurse, and care for offspring. roughly chronologically in relation to the timing of life history Although human beings share many characteristics with nonhuman stages—early development, puberty, mating, sex drive, motherhood, primates, we are unique in a number of ways. For instance, humans and menopause—and throughout we emphasize how hormones coordi- have a very long juvenile period and adult life span, both of which facil- nate life historical, contextual, and cyclic changes in women's reproduc- itate the acquisition of skills via cultural learning (Lancaster and Kaplan, tive anatomy, physiology, and behavior. Although much of what is 2009). Perhaps because of men's investment in offspring (which is un- known about these relationships in humans derives from clinical and usual among male mammals), women also engage in an extraordinary laboratory-based research, we highlight field-based research wherever level of mating competition (Campbell, 2013; Puts, 2010; Puts, 2016). possible. That is, as benefits conferred by men often cannot be shared among women, variation in male mate quality is predicted to engender female 2. Early development: sexual orientation and gender identity competition over high-quality males. This competition sometimes in- volves aggression and threats of aggression but generally takes the Two key elements of women's reproductive life history strategies form of mate attraction. are sexual orientation, the extent to which one is sexually attracted to Unlike most female primates, women exhibit relatively cryptic fer- men, women, or both (Hill et al., 2013; Rieger et al., 2005), and gender tile windows in their ovulatory cycles (Nunn, 1999), perhaps to prevent identity, one's feeling of being male, female, both, or neither (LeVay dominant males from monopolizing estrous copulations and thus to fa- and Baldwin, 2009). It is becoming increasingly evident that sexual ori- cilitate investment by subordinate males (Strassmann, 1981). However, entation and gender identity cannot be explained by gender socializa- there are several other adaptive explanations (see Haselton and tion alone, and that prenatal events are instrumental in their Gildersleeve, 2016), as well as byproduct explanations (e.g. Havlíček development. et al., 2015; but see Roney et al., 2015), for the evolution of concealed Consider the ideal experiment for investigating the role of gender ovulation in humans (see ESM). Women's sexual behavior is also un- socialization on psychosexual development: Begin with an infant of usual in that it extends across the ovulatory cycle. In most mammals, in- one sex and expose that child to a social environment typical of the op- cluding primates (e.g., Deschner et al., 2004; Nadler et al., 1983), female posite sex, including by changing the child's appearance so that others sexual activity is heightened during the fertile period of the reproduc- would perceive the child as the reassigned sex. Later, ascertain gender tive cycle (Beach, 1976; Dixson, 1998; Nadler et al., 1983; Thornhill identity and sexual orientation (Bailey et al., 2016). The larger the role and Gangestad, 2015). By contrast, evidence suggests that women's in- of gender socialization in psychosexual development, the more typical tercourse frequency tends to vary modestly and inconsistently, if at all, the child should be of the reassigned gender. across the ovulatory cycle (Baker and Bellis, 1995; Clayton et al., 1999; In fact, circumstances very close to this “ideal experiment” have oc- Matteo and Rissman, 1984; Udry and Morris, 1968; Wilcox et al., curred several times. Gender has been reassigned in several hormonally 2004). In combination with concealed ovulation, extended sexuality typical males whose penises were accidentally destroyed during cir- may have evolved in part because it enabled ancestral women to recruit cumcision, or were malformed due to cloacal exstrophy, in which the good genes surreptitiously from extra-pair males (Thornhill and abdomen and penis develop abnormally. The medical community Gangestad, 2015). However, the degree to which such “dual mating” once believed that such males would be happier being reassigned as fe- played a role in the evolution of these
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