Variability in energy expenditure is much greater in males than females

Abstract

In mammals, trait variation is often reported to be greater among males than females. However, to date, mainly only morphological traits have been studied. Energy expenditure represents the metabolic costs of multiple physical, physiological, and behavioral traits. Energy expenditure could exhibit particularly high greater male variation through a cumulative effect if those traits mostly exhibit greater male variation, or a lack of greater male variation if many of them do not. Sex differences in energy expenditure variation have been little explored. We analyzed a large database on energy expenditure in adult humans (1494 males and 3108 females) to investigate whether humans have evolved sex differences in the degree of interindividual variation in energy expenditure. We found that, even when statistically comparing males and females of the same age, height, and body composition, there is much more variation in total, activity, and basal energy expenditure among males. However, with aging, variation in total energy expenditure decreases, and because this happens more rapidly in males, the magnitude of greater male variation, though still large, is attenuated in older age groups. Considerably greater male variation in both total and activity energy expenditure could be explained by greater male variation in levels of daily activity. The considerably greater male variation in basal energy expenditure is remarkable and may be explained, at least in part, by greater male variation in the size of energy-demanding organs. If energy expenditure is a trait that is of indirect interest to females when choosing a sexual partner, this would suggest that energy expenditure is under sexual selection. However, we present a novel energetics model demonstrating that it is also possible that females have been under stabilizing selection pressure for an intermediate basal energy expenditure to maximize energy available for reproduction.

Keywords: Activity; Biological sex; DLW; Energetics; Trait variability.

Figure 1.

Male (closed circles) and female (closed triangles) variance for A) total energy expenditure (TEE), B) basal energy expenditure (BEE), and C) activity energy expenditure (AEE). While within sex variance differs considerably between TEE, BEE, and AEE, in each case, male variance is greater than female variance. Values shown are the posterior modes with 95% highest posterior density credible intervals (CI) for the sex-specific residual variance estimates extracted from models that did not include covariates (‘none’), and models that included three sets of covariates such as height and fat-free mass (set 1), height, fat-free mass, fat mass, and age (set 2), and height, fat-free mass, fat mass, age, and sex-specific nonlinear age and body composition effects (set 3). The open symbols show the variance estimates in females obtained from an analysis restricted to a data set in which sample size was randomly reduced to equal that of males.

Figure 2.

Histograms of total energy expenditure (TEE; AeC), basal energy expenditure (BEE; DeF), and activity energy expenditure (AEE; GeI) for adult males (dark grey) and females (light grey). A) Absolute TEE; B) TEE adjusted for height and fat-free mass (set 1); C) TEE adjusted for height, fat-free mass, fat mass, and age (set 2). D) Absolute BEE; E) BEE adjusted for height and fat-free mass (set 1); F) BEE adjusted for height, fat-free mass, fat mass, and age (set 2). G) Absolute AEE; H) AEE adjusted for height and fat-free mass (set 1); I) AEE adjusted for height, fat-free mass, fat mass, and age (set 2). In each panel, male variance is greater than female variance.

Figure 3.

Age-specific A) variance and B) coefficient of variance in total energy expenditure in males (circles) and females (triangles) and C) male:female variance ratio. The amount of greater male variability (GMV) remains fairly constant across age categories. Values shown are the posterior modes with 95% highest posterior density credible intervals (95% CIs) extracted from a single model that included multiple covariates and sex-specific nonlinear aging and body condition effects. Numbers shown below the symbols are the sample sizes for each category.

Figure 4.

Male (circles) and female (triangles) variance for total energy expenditure disaggregated into Western countries and non-Western countries. Values shown are the posterior modes with 95% highest posterior density credible intervals (CIs) for the sex-specific residual variance estimates extracted from models that included height, fat-free mass, fat mass, age, and sex-specific nonlinear age and body composition ef- fects, and country as a random factor. Numbers shown by the symbols are the sample sizes for each category. Variance in total energy expenditure among males is much higher in Western than non-Western countries, whereas the variance among females is similar in Western and non-Western countries; thus, the magnitude of greater male variability is decreased in non-Western countries.

Figure 5.

Conceptual model of energy availability during pregnancy in relation to basal energy expenditure (BEE). A) Sustained maximal energy expenditure is a multiple of BEE. Consequently, the energy potentially available for reproduction (calculated as sustained maximal energy expenditure minus BEE) is higher in females with a higher BEE. B) If food availability is limited, then energy intake can create a limit to sustained maximal energy expenditure (dashed line) and in turn, energy available for reproduction is not only low for females with a low BEE but also for females with a high BEE; it is highest when BEE is an intermediate value. The arrows denote selection against the extremes of low BEE and high BEE.