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1. See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/322644633 Testosterone Chapter · January 2018 DOI: 10.1007/978-3-319-16999-6_229-1 CITATIONS 0 READS 1,189 2 authors: Brian M. Bird Simon Fraser University Samuele Zilioli Wayne State University 20PUBLICATIONS   198CITATIONS    43PUBLICATIONS   470CITATIONS    SEE PROFILE SEE PROFILE All content following this page was uploaded by Brian M. Bird on 22 January 2018. The user has requested enhancement of the downloaded file.

2. T Testosterone characteristics), psychology (e.g., sexual desire), and behavior (e.g., aggression)—each of which plays an important role in survival and reproduc- tion. Testosterone effects clearly manifest during puberty when its levels rise significantly. How- ever, after puberty, short-lived testosterone fluctu- ations continue to affect some of these processes (e.g., aggression and sexual desire). Such fluctua- tions take place in response to environmental inputs, including changes in temperature, interac- tions with potential mates, and competitive exchanges. This entry will provide an overview of testosterone by briefly discussing its history and mechanisms (e.g., followed by a review of theoretical and empirical approaches to understanding how it may be impli- cated in behavioral processes that are critical to fitness optimization. Brian M. Bird1and Samuele Zilioli2,3 1Department of Psychology, Simon Fraser University, Burnaby, BC, Canada 2Department of Psychology, Wayne State University, Detroit, MI, USA 3Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, MI, USA Synonyms production, action), Androgen; Androgenic hormone; Endocrinology; Sex hormone; Steroid hormone Definition History and Mechanisms A steroid hormone present in various species, often in much greater quantities in males than females. In evolutionary psychology and endocri- nology, testosterone is thought to play a key role in mediating life history trade-offs. The discovery of testosterone’s role in under- standing behavior is often traced back to one of the first experiments in the field of behavioral endocrinology, published in 1849. In his work, Arnold Berthold castrated two roosters and dem- onstrated that the removal of the testes suppressed the development of secondary sexual characteris- tics (e.g., the comb and wattle), aggressive behav- ior toward other males, Interestingly, Berthold roosters and found that by reimplanting one testis Introduction Testosterone is a steroid hormone involved in many bodily processes, including reproductive physiology (e.g., spermatogenesis), morphology (e.g., development of and crowing. two castrated other secondary sexual # Springer International Publishing AG 2017 T.K. Shackelford, V.A. Weekes-Shackelford (eds.), Encyclopedia of Evolutionary Psychological Science, https://doi.org/10.1007/978-3-319-16999-6_229-1

3. 2 Testosterone Testosterone and Life History Theory in the abdominal cavity of each bird (with vascu- lar and neural connections severed), the birds managed to develop the typical characteristics of an intact rooster (e.g., crowing, growth of combs, engaging in confrontations). Because the testes continued to function normally despite being detached from vascular and neural connections, Berthold concluded that the testes must secrete some chemical that influences morphological development and behavioral Berthold had just discovered testosterone. Through several enzymatic steps, testosterone is synthesized from cholesterol in numerous tis- sues, including the testes, ovaries, and adrenal glands. Testosterone secretion is ultimately governed by the hypothalamic-pituitary-gonadal (HPG) axis. In men, testosterone secretion results from a hormonal “cascade,” where the pulsatile release of gonadotropin-releasing (GnRH) from the hypothalamus luteinizing hormone (and follicle-stimulating hor- mone) from the anterior pituitary gland, which in turn stimulates testosterone pulses from the Leydig cells in the testes. In women, testosterone is primarily secreted in the ovaries, which contain cells similar to those of the testes. Regardless of where it originates, testosterone acts on target cells through genomic and non- genomic mechanisms. Genomic mechanisms refer to the ability of unbound testosterone to cross the cell membrane, bind to the androgen receptor found in the cytoplasm of the cell, and migrate to the nucleus, where gene transcription can be activated or repressed. Once in the cell, testosterone can also be converted to other sex steroids, such as estradiol (via enzyme aromatase) or dihydrotestosterone a-reductase), which in turn bind to steroid hor- mone receptors and affect cell functioning. Genomic mechanisms are considered “slow,” meaning that the effects of testosterone take lon- ger to manifest (e.g., >30 min, up to hours, or even days). Non-genomic mechanisms, on the other hand, are rapid effects (e.g., <30 min) that do not involve gene transcription but instead an interaction between testosterone and cell mem- brane receptors (e.g., GABAAreceptors). In evolutionary biology, life history theory refers to the resource trade-offs faced across the lifespan by species trying to maximize reproductive fit- ness. The premise of life history theory is that resources (e.g., energy, time, nutrients) are lim- ited, and thus when they are invested into one trait to promote fitness, there is less available to invest in other fitness-promoting traits. Testosterone plays a key role in mediating some of the behav- ioral, physiological, and morphological processes that are inherent to life history trade-offs, such as copulation and courtship, sperm maturation, mus- cle growth and maintenance, immune function, and metabolism (Hau and Wingfield 2011). functioning. Mating Versus Parenting Trade-Off hormone stimulates One of the most studied life history trade-offs thought to be mediated by testosterone is mating effort versus parenting effort. Seminal work by John Wingfield (i.e., “The Challenge Hypothe- sis”; see Wingfield 2017, for review) found sea- sonal fluctuations of testosterone in avian species. While androgen levels were the lowest during the nonbreedingseason,theirlevelsroseatthestartof the breeding season. This increase in testosterone was necessary to promote spermatogenesis, the expression of secondary sexual characteristics, and reproductive behavior. During the rest of the breeding season, androgens reached a physiolog- ical maximum in response to intrasexual encoun- ters that birds had to face when protecting their territories. One important Wingfield’s work was that theexpression ofpater- nal care required temporary decreases in testoster- one secretion, providing preliminary evidence for testosterone’s role in mediating mating versus parenting trade-offs. Following from Wingfield’s work in avian spe- cies, research in humans showed that testosterone levelsvaryasafunctionofrelationshipandfather- hood status. For example, Gettler et al. (2011) followed a large sample of men (N = 624) for nearly 5 years and examined the extent to which partnering (i.e., married finding from (via enzyme 5- or cohabitating),

4. Testosterone 3 2015), in response to mating-relevant stimuli (reviewed in Roney and Gettler 2015), and drops following nurturant interactions with offspring (Kuo et al. 2016). Importantly, these rapid changes in testosterone to various social stimuli (competition, mating, parenting) seem to map onto future behaviors in these same domains. For example, testosterone responses to competi- tion influence the decision to compete again, future competitive performances, aggression, risk-taking, and courtship behaviors (Carré and Olmstead 2015; Zilioli and Bird in press). How testosterone is influenced by and influ- ences social behaviors can be modified by situa- tional, motivational, and physiological factors. In other words, the strength or direction of the bidi- rectional relationship between testosterone and social behavior changes as a function of modera- tors. Briefly, situational moderators refer to exter- nal factors that are not easily controlled, such as winning or losing a competition, with experiences of social victory being associated with an increase in testosterone relative to losing (see Mazur 1985, for this prediction from the “Biosocial Model of Status”; see Geniole et al. 2017, for meta- analysis). Motivational moderators refer to indi- vidual differences in psychological variables such as personality (e.g., dominance) or mating prefer- ences (e.g., sociosexual orientation). Finally, physiological moderators refer to the interaction of testosterone with other hormones and signaling molecules, such as cortisol, which has been found to attenuate the relationship between testosterone and behavior (see Mehta and Prasad 2015, for review of this “Dual-Hormone Hypothesis”). fatherhood,andpaternalcaregivingwereprospec- tively associated with testosterone levels. Single and childless men with elevated morning testos- terone levels at the beginning of the study were more likely to become newly partnered and newly partnered with children 4.5 years later. Further, men who became newly partnered with children by follow-up showed a greater decline in testos- terone from the beginning to the end of the study, when compared with men who remained single andchildlessthroughoutthestudy.Additionally,a comparison of childcare investment showed that fatherswhoweremostinvolvedinthecareoftheir children hadsignificantlylowertestosteroneatthe end of the study than fathers who did not partici- pate in offspring care. Other studies showed that men with higher testosterone tend to experience less satisfactory romantic relationships and higher rates of divorce, while lower testosterone levels have been associated with greater parental involvement (reviewed in Roney and Gettler 2015; see also Zilioli and Bird in press). These shifts in testosterone may be adaptive: on one hand, reduced levels may promote investment in successful relationships with close others (e.g., less risk of defection, greater care, and likelihood of offspring survival) and, on the other hand, elevated concentrations may promote behavior aimed at securing mates (e.g., mate seeking, extra-pair desires). Basal (i.e., at rest) levels of testosterone have been found to map onto traits inherent to repro- ductive success; however, testosterone concentra- tions are not static. On the contrary, testosterone fluctuates quite rapidly in response to environ- mental inputs and in patterns that are consistent with the predictions of the life history theory. Specifically, it has been hypothesized that situa- tions involving mating effort directly (such as interactions with a mate) or indirectly (such as intrasexual competition) lead to an increase in testosterone, while interactions involving parent- ing effort (such as nurturant parent-offspring interactions) lead to suppressed testosterone release or a testosterone decline (Zilioli and Bird in press). Empirical evidence indicates that testos- terone is released both in anticipation and in response to competitions (see Carré and Olmstead Conclusion As briefly reviewed, testosterone is implicated in numerous processes that are critical to reproduc- tion and survival, including the expression of secondary sexual characteristics, mate seeking, aggression, and status seeking. From an evolu- tionary perspective, testosterone’s role in promot- ing reproductive fitness can be explained largely from the framework of the life history theory, which proposes that species face evolutionary

5. 4 Testosterone trade-offs (e.g., mating versus parenting) due to the limited availability of resources (e.g., energy, time). Some of these trade-offs are mediated by testosterone. Future work in evolutionary endo- crinology and psychology will be needed to shed light on the situational, motivational, and physio- logical moderators of the relationship between (1) basal testosterone and behavior, (2) exposure to social stimuli and acute testosterone release, and (3) acute testosterone release and social behavior. Geniole, S. N., Bird, B. M., Ruddick, E. L., & Carré, J. M. (2017). Effects of competition outcome on testosterone concentrations in humans: An updated meta-analysis. Hormones and behavior, 92, 37–50. https://doi.org/10. 1016/j.yhbeh.2016.10.002. Gettler, L. T., McDade, T. W., Feranil, A. B., & Kuzawa, C. W. (2011). Longitudinal evidence that fatherhood decreases testosterone in human males. Proceedings of the National Academy 16194–16199. 1105403108. Hau, M., & Wingfield, J. C. (2011). Hormonally regulated trade-offs: Evolutionary variability and phenotypic plasticity in testosterone signaling pathways. In T. Flatt & F. Heyland (Eds.), Mechanisms of life history evolution. The genetics and physiology of life history traits and trade-offs (pp. 349–362). New York: Oxford University Press. Kuo, P. X., Saini, E. K., Thomason, E., Schultheiss, O. C., Gonzalez, R., & Volling, B. L. (2016). Individual var- iation in fathers’ testosterone reactivity to infant dis- tress predicts parenting behaviors with their 1-year-old infants. Developmental 303–314. https://doi.org/10.1002/dev.21370. Mazur, A. (1985). A biosocial model of status in face-to- face primate groups. Social Forces, 64(2), 377–402. 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. https://doi.org/10.1016/j.cobeha.2015.04.008. Roney, J. R., & Gettler, L. T. (2015). The role of testoster- one in human romantic relationships. Current Opinion in Psychology, 1, 81–86. https://doi.org/10.1016/j. copsyc.2014.11.003. Wingfield, J. C. (2017). The challenge hypothesis: Where it began and relevance to humans. Hormones and Behavior, 92, 9–12. https://doi.org/10.1016/j.yhbeh. 2016.11.008. Zilioli, S., & Bird, B. M. (in press). Functional significance of men’s testosterone reactivity to social stimuli. Fron- tiers in Neuroendocrinology. https://doi.org/10.1016/j. yfrne.2017.06.002. of Sciences, 108(39), https://doi.org/10.1073/pnas. Cross-References ▶Biosocial Perspective ▶Dominance and Testosterone ▶Dominance, Testosterone, and Cortisol ▶Female Mate Choice (Intersexual Selection) ▶Inclusive Fitness ▶Intrasexual Rivalry Among Men ▶Life History Strategies, Life History Theory, Secondary Sexual Characteristics ▶Parental Effort vs. Mating Effort ▶Parental Investment Theory ▶Sexual Selection ▶Survival and Reproduction Psychobiology, 58(3), References Carré, J. M., & Olmstead, N. A. (2015). Social neuroen- docrinology of human aggression: Examining the role of competition-induced testosterone dynamics. Neuro- science, 286, 171–186. https://doi.org/10.1016/j.neuro science.2014.11.029. View publication stats View publication stats