Age-independent increases in male salivary testosterone during horticultural activity among Tsimane forager-farmers

Abstract

Testosterone plays an important role in mediating male reproductive trade-offs in many vertebrate species, augmenting muscle and influencing behavior necessary for male–male competition and mating-effort. Among humans, testosterone may also play a key role in facilitating male provisioning of offspring as muscular and neuromuscular performance is deeply influenced by acute changes in testosterone. This study examines acute changes in salivary testosterone among 63 Tsimane men ranging in age from 16 to 80 (mean 38.2) years during one-hour bouts of tree-chopping while clearing horticultural plots. The Tsimane forager-horticulturalists living in the Bolivian Amazon experience high energy expenditure associated with food production, have high levels of parasites and pathogens, and display significantly lower baseline salivary testosterone than age-matched US males. Mixed-effects models controlling for BMI and time of specimen collection reveal increased salivary testosterone (p < 0.001) equivalent to a 48.6% rise, after one hour of tree chopping. Age had no effect on baseline (p = 0.656) or change in testosterone (p = 0.530); self-reported illness did not modify testosterone change (p = 0.488). A comparison of these results to the relative change in testosterone during a competitive soccer tournament in the same population reveals larger relative changes in testosterone following resource production (tree chopping), compared to competition (soccer). These findings highlight the importance of moving beyond a unidimensional focus on changes in testosterone and male–male aggression to investigate the importance of testosterone–behavior interactions across additional male fitness-related activities. Acutely increased testosterone during muscularly intensive horticultural food production may facilitate male productivity and provisioning.

Introduction

Testosterone is considered a primary mediating factor in male life history trade-offs, implicated in mate-seeking behaviors, territoriality, and secondary sexual characteristics, at a cost to paternal behavior and maintenance of immune function (Hau, 2007, Wingfield et al., 1990). Consistent with this evolutionary model, human studies find evidence for positive associations between testosterone and various aspects of mating effort including male–male competition (Archer, 2006), aggression (Archer, Birring, & Wu, 1998), and attracting mates (Roney, Hanson, Durante, & Maestripieri, 2006), with negative associations between testosterone and parenting effort (Gettler et al., 2011, Muller et al., 2009). The pattern of hormone-behavior interactions resulting in increased testosterone during male–male competition, and decreased testosterone when rearing offspring is commonly discussed under the framework of the “challenge hypothesis” (Archer, 2006, Goymann et al., 2007, Wingfield et al., 1990). The acute portion of the challenge hypothesis, as applied to human males, suggests that testosterone levels are maintained at relatively low levels to avoid the energetic and health costs of high testosterone, but spike when men engage in reproductively important behaviors including male–male competition and sexual activity in order to provide immediate muscular and behavioral advantages (Archer, 2006). While physical confrontations among males provide reproductive access to females in many mammals (Geary, 2000), human males often rely on different behavioral strategies to attract and maintain relationships with mates, tending to focus more on resource production, long-term investment in offspring, and competitive displays than on agonistic male–male interactions (Kaplan et al., 2000, Pillsworth, 2008, von Rueden et al., 2011).

Resource production is an important predictor of male reproductive success in subsistence and industrialized populations (Borgerhoff-Mulder and Beheim, 2011, Fieder and Huber, 2007, Gurven and Hill, 2009, Gurven and von Rueden, 2006, Hopcroft, 2006, Smith, 2004). Much of male food production involves the use of energy-intensive production techniques to obtain nutritionally dense but hard to acquire food resources, hallmarks of the human feeding niche (Kaplan et al., 2000). Testosterone promotes muscle growth and maintenance (Bribiescas, 2001), which are not only important in male–male competition, but also vital for physically active food production strategies that would have been the norm throughout most of human evolutionary history.

Although male–male aggression indisputably played a role in human evolution, there are numerous extant, historical, and archaeological examples of social regulations designed to reduce the damage caused by male–male violence, ranging from axe and club fight protocols to state laws (Daly and Wilson, 1988, Hill and Hurtado, 1996, Hill et al., 2009). The coevolution of the human feeding niche, longevity, and brain size may have applied a different set of selective pressures on the role of testosterone in humans, where males who tend to place a greater emphasis on resource production and paternal care than on direct competition when compared to other male mammals (Geary, 2000, Hill et al., 2009, Kaplan et al., 2000). Increases in male productivity can help maximize reproductive success by improving offspring survivorship, partner fecundity and greater selectivity in the mating market (Gurven & von Rueden, 2006; Kaplan and Hill, 1984; Smith, 2004). Thus acute increases in testosterone may be one strategy to gain the performance benefits associated with high testosterone, while avoiding the behavioral and immunocompromising effects of high baseline testosterone. This study looks beyond male–male competition to examine changes in testosterone during horticultural activity, and argues for extending the role of testosterone for improving reproductive success by helping to maximize productivity, rather than through traditional male–male competition.

In industrialized populations, male testosterone peaks in the early twenties and declines with age (Harman et al., 2001, Uchida et al., 2006, Travison et al., 2007). Declines in testosterone among men in industrialized populations have been linked to inflammation, obesity, metabolic disorders, and other age-linked diseases of affluence (Travison et al., 2007). The Tsimane, and other non-industrialized populations facing energetic constraints and pathogenic stress show lower levels of testosterone across all adult ages as compared with men in industrialized nations, (Bribiescas, 1996, Bribiescas and Hill, 2009, Ellison et al., 2002, Trumble et al., 2012, Vitzthum et al., 2009, Worthman and Konner, 1987), as well a slower and shallower rate of change with age (Ellison et al., 2002), or no association between testosterone and age (Bribiescas, 1996, Trumble et al., 2012, Vitzthum et al., 2009). Male production needs to remain high throughout life in order to provision offspring and grand-offspring; thus, we predict that men in subsistence-based societies, including the Tsimane, will be able to sustain acute increases in testosterone during horticultural activity across the adult life course.

Small-scale slash-and-burn horticulture conducted by Tsimane males offers the opportunity to examine changes in testosterone during tree chopping, a controlled, intense, non-competitive physical activity. Do Tsimane men express acute changes in testosterone during physical activity similar to the effects of comparable physical activity in industrial populations? Does competitive physical activity produce a greater increase in testosterone than physical activity alone? This study expands the hormone-behavior interaction literature beyond male–male competition and aggression to better understand the importance of acute testosterone–behavior interactions outside of mating-effort, specifically changes in testosterone during tree-chopping for small-scale horticulture.

Despite having salivary testosterone levels one-third lower than age-matched US males (Trumble et al., 2012), Tsimane men engage in production strategies requiring significant muscle mass and cardiovascular performance. The primary hypothesis of this study is that testosterone will increase significantly during physical activity, despite lower overall levels of testosterone. Exhibiting acute increases in testosterone during physical activity may serve to increase and maintain muscle mass, while still allowing Tsimane men to reap the energetic and immune benefits of low baseline testosterone.

A previous study reported acutely increased testosterone during a soccer tournament among Tsimane men (Trumble et al., 2012). If competition is a main driver of acute changes in testosterone, then we would expect tree chopping to result in a smaller change in testosterone in comparison to the soccer tournament. However, if acute changes in testosterone are largely due to physical activity, then we would expect equivalent changes in testosterone during both activities.