Selection of endurance capabilities and the trade-off between pressure and volume in the evolution of the human heart

Abstract

Chimpanzees and gorillas, when not inactive, engage primarily in short bursts of resistance physical activity (RPA), such as climbing and fighting, that creates pressure stress on the cardiovascular system. In contrast, to initially hunt and gather and later to farm, it is thought that preindustrial human survival was dependent on lifelong moderate-intensity endurance physical activity (EPA), which creates a cardiovascular volume stress. Although derived musculoskeletal and thermoregulatory adaptations for EPA in humans have been documented, it is unknown if selection acted similarly on the heart. To test this hypothesis, we compared left ventricular (LV) structure and function across semiwild sanctuary chimpanzees, gorillas, and a sample of humans exposed to markedly different physical activity patterns. We show the human LV possesses derived features that help augment cardiac output (CO) thereby enabling EPA. However, the human LV also demonstrates phenotypic plasticity and, hence, variability, across a wide range of habitual physical activity. We show that the human LV's propensity to remodel differentially in response to chronic pressure or volume stimuli associated with intense RPA and EPA as well as physical inactivity represents an evolutionary trade-off with potential implications for contemporary cardiovascular health. Specifically, the human LV trades off pressure adaptations for volume capabilities and converges on a chimpanzee-like phenotype in response to physical inactivity or sustained pressure loading. Consequently, the derived LV and lifelong low blood pressure (BP) appear to be partly sustained by regular moderate-intensity EPA whose decline in postindustrial societies likely contributes to the modern epidemic of hypertensive heart disease.

Keywords: blood pressure; human evolution; left ventricle; physical activity; trade-off.

Fig. 1.

Comparison of the LV structure and the function in chimpanzees and 2 representative human groups: sedentary Americans and Tarahumara subsistence farmers. (A–C) Scaled outlines of LVs among the 3 groups highlighting differences in trabeculation, WT, chamber size, and shape. (D) Basal and apical systolic (shaded) and diastole (unshaded) rotation. (E) Magnitude of LV twisting, untwisting, and the respective velocities during systole (shaded) and diastole (unshaded). While chimpanzees lack apical rotation and, thus, overall systolic twist, sedentary humans and subsistence farmers have similar levels of systolic twisting and early diastolic UTVs.

Fig. 2.

Comparison of the LV structure and the function among chimpanzees and 4 human groups with diverse physical activity histories. (A and B) Principal component analysis of LV variables determined a priori to be associated with either pressure (A) or volume (B) exposure. Principal component scores are expressed as standardized Z scores. (C and D) General linear model of first principal component scores for pressure (C) and volume (D) regressed on group identity with means and 95% confidence intervals. Groups analyzed: chimpanzees (CHI); sedentary Americans (SAM); American-style football linemen (AFL); long-distance runners (LDR); and Tarahumara subsistence farmers (TAR). Pressure variables are as follows: peak systolic LV tissue velocity (S′), Mid-LV Mid RWT, basal-LV RWT, Mid-LV Mid WT, SBP, DBP; volume variables are early diastolic transmitral valve blood flow velocity (MVE), peak early diastolic tissue velocity (E′), SI, CO, SV, LVL, LV EDV, LV ESV, LV OT diameter. All ventricular structural data entered into the analyses were scaled as per SI Appendix.

Fig. 3.

Trade-off between EPA and RPA training on the LV structure and function. (A) After 90 d of intensive training, the EPA athletes demonstrated eccentric LV remodeling characterized by increases in LV chamber volume (∆ EDV = 7%, ∆ RWT = −3%) and improved diastolic function (∆ E′ = 12%) while the RPA athletes demonstrated concentric remodeling characterized by (∆ WT = 13%, ∆ RWT = 8%) and reduced diastolic function (∆ E′ = −7%). (B) Relationship between RWT and LV SV in response to volume challenge (Top) and pressure challenge (Bottom) among these athletes after training. RPA-trained athletes with relatively thicker LV walls were less able than EPA-trained athletes to increase SV (∆SV = 6% vs. ∆SV = 16%) when challenged with rapid intravascular infusion of normal saline. In contrast, RPA-trained athletes were better able to preserve SV (∆SV = −4%) when pressure challenged with an isometric grip test than EPA-trained athletes (∆SV = −21%).

Fig. 4.

Difference in SBP (solid line) and DBP (dashed line) in male chimpanzees, Tarahumara subsistence farmers, and sedentary Americans (NHANES data). Tarahumara subsistence farmers (blue) and sedentary Americans (green) are presented relative to age (shaded areas indicate 95% confidence interval of the mean), whereas a point estimate of mean BP relative to mean age is provided for the smaller chimpanzee cohort (red). Although BP increases with age in the NHANES sample, this is not apparent in the Tarahumara.