Surgent, dominant, and athletic men could possess a greater ability to regulate oxidative stress; women whose faces were judged as more attractive also had higher oxidative stress, a possible cost of maintaining this phenotype

Oxidative stress and the differential expression of traits associated with mating effort in humans. Nicholas M. Grebe et al. Evolution and Human Behavior, March 13 2021. https://doi.org/10.1016/j.evolhumbehav.2021.02.007

Abstract: Oxidative stress is a physiological condition in which reactive oxygen species created through cellular respiration can potentially damage DNA and tissue. Oxidative stress may partially mediate trade-offs between reproductive effort and survival efforts. On the one hand, traits associated with reproductive effort, particularly costly male-male competition, are expected to raise oxidative stress. On the other hand, behavioral strategies may be a critical mediating mechanism, such that those who can better resist the physiological costs of oxidative damage exhibit increased mating effort. In a sample of 248 college students (173 men), we examined the associations between traits linked to mating effort—including personality features, athleticism, and history of illness—with levels of 8-OHdG, a biomarker of oxidative stress. 8-OHdG was measured twice, one week apart, once during active hours and once at awakening. In men, surgency, social dominance, and athleticism were all negatively associated with 8-OHdG levels in awakening, but not lab samples collected during active hours. In women, these same traits were positively associated with 8-OHdG levels, particularly in morning samples. Differences in associations based on sex and time of collection introduce additional complexities to understanding links between oxidative stress and mating effort.

Keywords: Oxidative stressMating effortHuman biologyPersonality

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4. Discussion

4.1 Summary of Associations

Our study explored two alternative scenarios for associations between oxidative stress and putative measures of investment in mating effort. On one hand, surgent, dominant, and athletic men could possess a greater ability to regulate oxidative stress, reflected by lower levels of 8-OHdG, consistent with associations found in rhesus macaques (Georgiev et al., 2015); on the other hand, high activity levels of these men could produce associations in the opposite direction. As a comparison, we investigated these same features in women, predicting weaker or absent associations. Our results showed that surgent, dominant, and athletic men tended to produce low levels of 8-OHdG in first-of-the-morning urine. Provisionally, we interpret this pattern to have one or both of two explanations. First, surgent, dominant, and athletic men may experience relatively little oxidative damage throughout the day to be repaired. Second, surgent, dominant, and athletic men may experience relatively little oxidative damage as a function of basal metabolic processes experienced overnight. In turn, these associations may be attributable to multiple underlying processes, including a smaller number of ROS-producing mutations and/or relatively low levels of environmental toxins. In either of these scenarios, men’s surgency, dominance, and athleticism partly reflects underlying condition—fundamentally, the capacity to efficiently convert energy into fitness-enhancing activity. An explanation for these associations may lie in the role of oxidative stress in the production of sexually selected signals. Individuals who suffer lower costs to energy production in the form of oxidative stress will be selected to energetically invest, over development, more heavily in capacities resulting in surgency, social dominance, and athleticism.

By contrast, women’s surgency, social dominance, and athleticism positively covaried with levels of 8-OHdG measured in urine collected at awakening. Why do women show a very different pattern? The pattern for men in the scenarios above results from selection for investment in traits (i.e., surgency, dominance, and athleticism) that may boost mating success in men that can physiologically “afford” them due to efficient oxidative stress regulation. To some degree, despite sex differences, women may have ancestrally benefited from investments in developing these phenotypes, too. At the same time, there is reason to suspect that these investments would not have been contingent on condition in the same way we propose they would have been for men. If women who possess relatively high levels of surgency, dominance, and athleticism are not ones who pay low costs for energy production in the form of oxidative stress, there is no reason to expect negative associations between them and oxidative stress. And indeed, because these traits—and many others that reflect increased mating effort—may be associated with higher levels of energy production, one might expect that women who possess them generate greater levels of ROS, which would result in greater oxidative damage and greater need for repair. One recent study presents evidence consistent with this notion: women whose faces were judged as more attractive also had higher oxidative stress, suggesting a possible cost of maintaining this phenotype (Marcinkowska et al., 2020). (By contrast, Gangestad et al. [2010] found male facial attractiveness to covary positively with a biomarker of oxidative stress; Foo et al. [2017] did not detect an association for either sex.)

We emphasize that these interpretations are provisional and require corroboration, both via direct replication, and via extensions that collect additional phenotypic information pertaining to mating effort (e.g., anthropometric measurements). We offer them because they may lead to fruitful directions for future research At the same time, in light of the complexities of associations between sexual signals, reproductive effort, and oxidative stress, some of which we reviewed in the introduction, we fully recognize that alternative explanations are possible. Furthermore, consistent with the notion that there is still much to be resolved in this literature, we also find unexpected, major differences in patterns based on when and how oxidative stress biomarkers are sampled, which we discuss below.

4.2 Implications for Understanding the Moderating Effect of Collection Time

Strong sex-specific associations between personality/health and oxidative stress were qualified by time of sampling. For men, negative associations of surgency, social dominance, and athleticism with levels of 8-OHdG measured in awakening samples disappeared when examining samples collected during lab sessions later in the day. Surgent, dominant, and athletic women had relatively high levels of 8-OHdG in both awakening and active samples, though associations were weaker in the latter set of samples.

One can reasonably ask whether these moderation effects are robust and meaningful. There are several reasons to think that they are. First, moderation by sex and sample was significant and consistent across three related factors (surgency, dominance, athleticism). Second, in analyses that substituted time since awakening for the crude binary of “sampling session”, moderation effects consistently strengthened, supporting the interpretation that this is the relevant difference driving effects. Third, our results remained similar in analyses predicting log-transformed 8-OHdG concentrations, suggesting outliers were not responsible for our observed pattern of effects. Finally, we observed a similar moderation effect for uric acid: effects differed between awakening and lab sessions (though, in this instance, this interaction was not moderated by sex). This effect of uric acid was independent from the effects of surgency, dominance, and athleticism. Nonetheless, the fact that time since awakening moderated this effect too bolsters the idea that time of sampling importantly moderates associations with 8-OHdG. While further studies are needed to establish the robustness and generalizability of these moderation effects, below we offer our provisional interpretation of what they might reflect in our studies.

Concentrations of 8-OHdG in urine do not capture instantaneous levels. Rather, they reflect the accumulation of 8-OHdG filtered out of circulating blood by the kidneys and stored in the bladder between last void and current void. For a first-morning void, this time span consists of a long, inactive period—sleep. By contrast, urine collected during daytime hours has largely accumulated during relatively short, active periods. Based on this observation, perhaps the most straightforward explanation for diverging associations is that an awakening measure of oxidative stress represents a more stable, and thus desirable, estimate of accumulated damage compared to daytime samples more affected by metabolic demands of daily activities (e.g., exercise). The fact that medical biomarker research favors first-morning voids for similar reasons (e.g. Witte et al., 2009; Heerspink et al., 2010) supports this interpretation.

We do entertain a second interpretation that specifically implicates sleep. Much somatic repair occurs during sleep, and indeed, one primary function of sleep across a wide range of taxa may be to permit allocation of energy to repair processes for oxidative damage (Anafi et al., 2013). At the same time, sleep itself slows the accumulation of oxidative damage, as the rate of metabolic expenditure slows. From this reasoning, it follows that someone with relatively low levels of 8-OHdG accumulated during sleep (i.e., found in first-morning voids) (a) experiences relatively low levels of oxidative damage throughout the day, to be repaired at night, and/or (b) produces relatively low levels of oxidative damage through basal metabolic processes. This interpretation is provisional and requires additional tests. We did not detect effects of sleep quality in our sample but future research may further investigate its impact.

4.2.1 Associations with Uric Acid

Because oxidative stress can be affected by the action of anti-oxidants, we considered whether concentrations of uric acid influenced the relationships we examined. While we did not find that uric acid mediated links between 8-OHdG and the traits we examined, we did find that uric acid covaried with 8-OHdG differently in awakening and active daytime samples, providing an independent piece of evidence that time of sampling affects associations with 8-OHdG. The effects of uric acid on oxidative damage can reverse, from anti-oxidant to pro-oxidant, in response to cellular environments (Sautin et al., 2007; So & Thorens, 2010), and prior evidence suggests that circadian rhythms have a strong influence on these roles (Stringari et al., 2015; Kono et al., 2010). Our examination of the role of anti-oxidants was limited in this study. Future research would benefit from considering a wider range of anti-oxidant assays, which can provide a triangulated estimate of different components underlying an organism’s anti-oxidant system (Constantini, 2011).

4.3 No Detected Associations with Susceptibility to Infectious Disease

In contrast to individual differences in surgency, social dominance, and athleticism, susceptibility to infectious disease did not substantially covary in our study with 8-OHdG, either in men or women, or in awakening or lab samples. Future research may examine these associations further, as well as assess associations between current infectious status and 8-OHdG levels. We note here that our results are based on two samples of young adults from a non-clinical, industrialized population. This poses a constraint on generalization for all of the conclusions we have presented, but it may be particularly relevant for measures of susceptibility to infectious disease. Clinical populations, unsurprisingly, have an elevated susceptibility to infectious disease (WHO, 2011), and distributions of immune function biomarkers and disease susceptibility differ markedly between industrialized and non-industrialized populations, which has important consequences for patterns of energetic investment (e.g. Blackwell et al., 2016). A broader sampling of the range of infectious disease burden in future research will permit a fuller examination of its role in oxidative stress and energetic trade-offs.