Selection for Sustained Aerobic Physical Activity Impacted Human Thoracic Form and Function

Abstract

Humans differ from other non-human primates, including chimpanzees, in being well-adapted for endurance rather than for power and speed. While chimpanzees walk 3-5 km per day with occasional rapid bursts of activity followed by intense panting, cooling, and resting, human hunter-gatherers typically walk approximately 5-15 km per day and often engage in other sustained aerobic physical activities. Furthermore, some humans have been documented to run long distances in order to persistence hunt during which they need to increase air intake as much as 1.3-2.5 L/min/kg of body mass. Few animals apart from humans are capable of such sustained aerobic capacity, which involves many adaptations, including the ability to exchange air rapidly and efficiently.

Despite the chest’s important involvement in ventilation, we know little about the evolution of the derived features of the human thorax that might contribute to these capabilities. Thus far, research concerning the evolution of human thoracic morphology has focused mainly on changes in overall thoracic shape and the transition from funnel-shaped to barrel-shaped chests in the hominin lineage, and there has been little research on differences in the thoracic movements involved in breathing during different forms of bipedal locomotion, such as walking and running. Furthermore, the differences in thoracic movements between humans, other endurance cursors, and non-cursorial mammals, as well as the differences in rib and vertebral anatomy that enable increased thoracic movement, remain unexplored. This thesis seeks to remedy this knowledge gap by focusing on the function, morphology, costs, and benefits of the human thorax during ventilation. This thesis tests the general hypothesis that the genus Homo evolved novel features in the thorax to increase ventilatory capacity as necessitated by increased oxygen demand, whether during endurance physical activity or in response low-oxygen environments.

The first study integrates experimental and comparative data to test whether selection has increased thoracic contribution to ventilation in endurance-adapted cursorial mammals, including humans. To do so, this study investigates whether humans and dogs increase thoracic contributions to ventilation during sustained aerobic activity more than a non-endurance species, goats. Furthermore, the study links derived costovertebral joint morphologies to increased rib mobility for thoracic expansion across four mammalian orders. The results show that endurance-adapted cursors use varying amounts of thoracic motion to increase thoracic ventilation, which corresponds with having increased concavo-convex costovertebral joint morphologies, while thoracic ventilation in non-endurance species is limited by their flattened costovertebral joint architecture. Evidence for similarly derived concavo-convex costovertebral joints in Homo erectus corresponds with the emergence of human endurance running and suggests that selection acted to increase ventilation in the genus Homo.

The second study addresses how much the ability to ventilate by expanding the thorax is phenotypically plastic in response to aerobic demand in modern humans. This study measures tidal volume, heart rate, and rib-motion in non-athletes, runners and swimmers while walking and running. Swimmers, who practice intermittent breathing while being aerobically active in an oxygen-limited environment, increased thoracic ventilation 1.4 to 2.0-times more than other participants. Runners were immediate, and non-athletes were least able to expand their chests when breathing. These differences indicate that human thoracic movement is highly phenotypically plastic in response to aerobic demand and is another line of evidence that selection favored the human ability to increase thoracic ventilation during endurance physical activities.

The third study uses a natural experiment to further explore how chest shape and movement contribute to ventilation in modern humans by assessing how adulthood acclimatization, developmental adaptation, and population-level adaptation to different altitudes affect breathing during sustained aerobic activity. Tidal volume, heart rate, and rib-motion during walking and running were measured in participants from lowland populations living in Boston (~35 m) and from high-altitude adapted Quechua participants born and living at sea-level (~150 m) and at high altitude (>4000 m) in Peru. Quechua participants, increased thoracic volume 2.0 to 2.2-times more than lowland participants, and Quechua individuals from hypoxic environments had deeper chests resulting in 1.3-times greater increases in thoracic ventilation than those at sea level. These results are evidence that increased thoracic ventilation derives from a combination of acclimatization, developmental adaptation, and population-level adaptation to aerobic demand in different oxygen environments.

The results of this thesis shed new light on ventilatory function of the chest within the broader context of the evolution of endurance physical activity in the genus Homo. The correlation between increased reliance on thoracic movement during ventilation while physically active and changes in costovertebral joint morphology, the substantial functional plasticity observed in thoracic ventilatory function in modern humans, and the clear evidence of developmental and population-level selection for increased thoracic ventilation in high-altitude populations all strongly support the hypothesis that selection for sustained aerobic physical activity acted on the thorax in the genus Homo. Selection for increased ventilation while physically active for long periods of time fundamentally changed one aspect of thoracic function in Homo and continues to impact physical activity in modern humans to this day.