Seasonal and circadian variation in salivary testosterone in rural Bolivian men

Abstract

Testosterone (T) plays a key role in the increase and maintenance of muscle mass and bone density in adult men. Life history theory predicts that environmental stress may prompt a reallocation of such investments to those functions critical to survival. We tested this hypothesis in two studies of rural Bolivian adult men by comparing free T levels and circadian rhythms during late winter, which is especially severe, to those in less arduous seasons. For each pair of salivary T(AM)/T(PM) samples (collected in a approximately 12-h period), circadian rhythm was considered classic (C(CLASSIC)) if T(AM) > 110%T(PM), reverse (C(REVERSE)) if T(PM) > 110%T(AM), and flat (C(FLAT)) otherwise. We tested the hypotheses that mean T(AM) > mean T(PM) and that mean T(LW) < mean T(OTHER) (LW = late winter, OTHER = other seasons). In Study A, of 115 T(PM)-T(AM) pairs, 51% = C(CLASSIC), 39% = C(REVERSE), 10% = C(FLAT); in Study B, of 184 T(AM)-T(PM) pairs, 55% = C(CLASSIC), 33% = C(REVERSE), 12% = C(FLAT). Based on fitting linear mixed models, in both studies T(OTHER-AM) > T(OTHER-PM) (A: P = 0.035, B: P = 0.0005) and T(OTHER-AM) > T(LW-AM) (A: P = 0.054, B: P = 0.007); T(PM) did not vary seasonally, and T diurnality was not significant during late winter. T diurnality varied substantially between days within an individual, between individuals and between seasons, but neither T levels nor diurnality varied with age. These patterns may reflect the seasonally varying but unscheduled, life-long, strenuous physical labor that typifies many non-industrialized economies. These results also suggest that single morning samples may substantially underestimate peak circulating T for an individual and, most importantly, that exogenous signals may moderate diurnality and the trajectory of age-related change in the male gonadal axis.

Figure 1

T_PM plotted against T_AM in 3 studies. Figure 1A=rural Bolivian men from Provincía Aroma (Study B); Figure 1B=rural Bolivian men from Provincía Murillo (Study A); Figure 1C=U.S. men from Spratt et al. (1988). Both axes are log₂ scale (nmol/L = 0.0347 ng/dL). Below the solid diagonal line, T_PM<T_AM (classic circadian rhythm); above the line, T_PM>T_AM (reverse circadian rhythm). The first pair of dotted lines either side of solid diagonal delineate T_AM/T_PM pairs defined as “flat” (T_AM=T_PM±10%). The second pair of dotted lines delineate T_AM=2T_PM (below the solid diagonal) and T_PM=2T_AM (above the solid diagonal). +=younger men, ●=older men (defined as above and below the median of each sample in Studies A and B; all men in Figure 1C are ≤ 37 years). In Figure 1A, 3 points outside the plotted area are not included to conserve space and increase clarity.

Figure 2

Distribution of individual circadian rhythm [defined as (log₂T_PM)–(log₂T_AM) in Study A and as [(log₂T_PM-MON + log₂T_PM-WED + log₂T_PM-FRI)/3] – [(log₂T_AM-MON + log₂T_AM-WED + log₂T_AM-FRI)/3)] in Study B] during late winter and during other seasons in Study A (left) and B (right). Diurnality <0 has higher T_AM than T_PM. Mean in each sample is indicated by a dashed line. There is substantial individual variation in diurnality in each sample and season. The seasonal difference in diurnality arises from a larger proportion of the sample having T_PM>T_AM in late winter than in other seasons (see text for additional discussion).