Seasonal variation of salivary testosterone in men, normally cycling women, and women using hormonal contraceptives
Highlights
► Little is known about humans' testosterone variation over long timescales (i.e., seasons). ► Men and normally-cycling (NC) women have significant seasonal testosterone variation. ► Men's and NC women's testosterone is maximal in the fall/winter and minimal in the spring/summer. ► Women using hormonal contraceptives have a flatter seasonal testosterone profile than NC women.
Introduction
Seasonal and circannual rhythms of physiology and behavior exist in a wide variety of species. Recurring seasonal environmental changes (e.g., photoperiod, temperature, plant growth/food availability) commonly result in changes in body mass, reproduction, immune function, foraging and food intake [23], [24]. These seasonally-driven changes in behavior track changes in physiology that are often regulated by the endocrine system. Testosterone has been shown to follow a seasonal rhythm in many species – particularly in males [5], [6], [8], [19] – that can promote changes in behavior (e.g., aggression, mating) [24], [39]. Some evidence links seasonal variation in testosterone to seasonal changes in human behavior [16] and physiology, such as waist-to-hip ratio [34], [38]. Since a number of behaviors are linked to testosterone in humans (e.g., cognitive abilities [20]; e.g., power and dominance competition [30], [33]; e.g., relationship status and sexual intercourse [36], [37]), accurately characterizing seasonal variation in humans' testosterone concentrations would have important implications for understanding seasonal variation in human behavior.
Like many mammals, humans' endogenous testosterone concentrations systematically vary over temporal scales ranging from days [7], [9], to months [7], to a lifespan [8]. While testosterone variation at short time scales (e.g., diurnal variation) is relatively well understood, the nature of long-time-scale variation (seasons and years) is much less well documented, particularly with regard to women. The few studies to be completed in humans have reported inconsistent findings and principally used male subjects. Not only have some found evidence of seasonal variation and some not, there are also inconsistencies in the peak and trough months of testosterone concentrations [34]. While the majority of studies report that testosterone concentrations peak in the fall for men (e.g., [21], [38]), others have reported peaks during other months of the year (e.g., [22], [35]). Inconsistencies in prior findings may have resulted from the varied nature of different studies: some used atypical populations (e.g., prepubertal children [2]; elderly men [22]), used participants of only one sex [8], [12], or collected samples over less than a full year [40]. Thus, the specific nature of the seasonal variation in humans' testosterone concentrations remains poorly characterized.
Studies of women's seasonal variation in testosterone are rare and have had conflicting findings. Considering the four existing studies of women: Garde et al. [12] found that serum testosterone peaked in summer months, both van Anders et al. [38] and Wisniewski and Nelson [40] found salivary testosterone peaked in the fall, and Moffat and Hampson [21] found no significant seasonal variation. Moreover, commonly-taken exogenous hormone treatments that affect sex steroid production and release, such as oral contraceptives, could be associated with alteration of seasonal testosterone variation in women. Hormonal contraceptive use is associated with suppression of women's endogenous testosterone concentrations [11], [28], as well as menstrual cyclicity of other steroids of ovarian origin, i.e., estradiol and progesterone [14].
Because of these effects of hormonal contraceptives on endogenous steroids, there is an ongoing debate within human behavioral endocrinology regarding the inclusion or exclusion of female human subjects on the basis of their use of exogenous hormonal contraception. Josephs [15] argued that not only should all female participants be included in such studies, but also that the field would benefit from trying to understand the effects of specific hormonal contraceptives on behavior and endocrine physiology. In contrast, since hormonal contraceptives are associated with reduced endogenous concentrations of steroid hormones including testosterone [11], [28], [31], other researchers have argued that normally-cycling women and women taking hormonal contraceptives should be treated as fundamentally different and analyzed separately, or hormonal contraceptive users should be excluded entirely from analyses [21], [36], [38]. Some studies have found that hormonal contraceptive use is associated with alteration of the relationship between basal testosterone and behavior [1], [13] and testosterone reactivity to social interactions [18], while others have not [11]. The extent to which hormonal contraceptive use alters other aspects of systematic variation in testosterone, e.g., seasonal variation, will further inform research on the behavioral correlates of testosterone in women. Thus, seasonal variation in women – whether using or not using hormonal contraceptives – remains an open and important topic for study.
The present study aimed to describe the seasonal variability in endogenous testosterone for both men and women, and also aimed to document effects of hormonal contraceptive use on said variability in women. We hypothesized that both men and normally-cycling women would show seasonal variation in testosterone concentrations. Furthermore, we hypothesized that hormonal contraceptive use would not only be associated with a reduction in women's endogenous testosterone concentrations, but would also be associated with a reduction in the peak-to-trough seasonal variation.
Section snippets
Participants
Seven hundred eighteen participants (299 men and 419 women; age range 18–66 y; M = 22.7 y, SD = 5.9 y) were recruited via flyers and through online subject participation websites. All participants provided informed consent under a protocol approved by the Duke University Medical Center Institutional Review Board. Participants with testosterone concentrations greater than 3 SDs from the mean within sex (N = 13) or with testosterone measurement coefficients of variation (CV) greater than 50% were excluded
Results
Table 1 reports the means, standard deviations and number of participants by month of endogenous testosterone concentrations for men, normally-cycling women, and women taking hormonal contraceptives. The grand means of testosterone were: men (N = 296), M = 77.5 (± 25.0) pg/mL; normally-cycling women (N = 262), M = 13.3 (± 5.6) pg/mL; and women taking hormonal contraceptives (N = 130), M = 8.5 (± 3.6) pg/mL.
Likely due to the small window of time of day during which saliva was collected [17], testosterone was
Discussion
Our first hypothesis that men and normally-cycling women would show significant seasonal variation in salivary testosterone concentrations was affirmed. Men had peak concentrations of testosterone in fall and lowest concentrations of testosterone in spring, which is generally consistent with past reports [8], [34]. Normally-cycling women showed a pattern of seasonal variation in testosterone that was similar to men, but they reached a peak annual testosterone concentration 2 months earlier
Acknowledgments
This research was supported by a Duke Institute for Brain Sciences Incubator Award (to S.A.H.), NIMH grant RC1-088680 (to S.A.H.), and the McClelland Postdoctoral Fellowship from the Hay Group (to S.J.S.). We thank R. Edward McLaurin and Rosie Phillips for their assistance with testing participants.
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