Comparing high versus low-altitude populations to test human adaptations for increased ventilation during sustained aerobic activity.

Despite aerobic activity requiring up to tenfold increases in air intake, human populations in high-altitude hypoxic environments can sustain high levels of endurance physical activity. While these populations generally have relatively larger chest and lung volumes, how thoracic motions actively increase ventilation is unknown. Here we show that rib movements, in conjunction with chest shape, contribute to ventilation by assessing how adulthood acclimatization, developmental adaptation, and population-level adaptation to high-altitude affect sustained aerobic activity. We measured tidal volume, heart rate, and rib-motion during walking and running in lowland individuals from Boston (~ 35 m) and in Quechua populations born and living at sea-level (~ 150 m) and at high altitude (> 4000 m) in Peru. We found that Quechua participants, regardless of birth or testing altitudes, increase thoracic volume 2.0-2.2 times more than lowland participants (p < 0.05). Further, Quechua individuals from hypoxic environments have deeper chests resulting in 1.3 times greater increases in thoracic ventilation compared to age-matched, sea-level Quechua (p < 0.05). Thus, increased thoracic ventilation derives from a combination of acclimatization, developmental adaptation, and population-level adaptation to aerobic demand in different oxygen environments, demonstrating that ventilatory demand due to environment and activity has helped shape the form and function of the human thorax.

Thoracic adaptations for ventilation during locomotion in humans and other mammals.

Bipedal humans, like canids and some other cursorial mammals, are thought to have been selected for endurance running, which requires the ability to sustain aerobic metabolism over long distances by inspiring large volumes of air for prolonged periods of time. Here, we tested the general hypothesis that humans and other mammals selected for vigorous endurance activities evolved derived thoracic features to increase ventilatory capacity. To do so, we investigated whether humans and dogs rely on thoracic motion to increase tidal volume during running to a greater extent than goats, a species that was not selected for endurance locomotion. We found that while all three species use diaphragmatic breathing to increase tidal volume with increasing oxygen demand, humans also use both dorsoventral and mediolateral expansion of the thorax. Dogs use increased dorsoventral expansion of the thorax, representing an intermediate between humans and goats. 3D analyses of joint morphology of 10 species across four mammalian orders also showed that endurance-adapted cursorial species independently evolved more concavo-convex costovertebral joint morphologies that allow for increased rib mobility for thoracic expansion. Evidence for similarly derived concavo-convex costovertebral joints in Homo erectus corresponds with other evidence for the evolution of endurance running in the genus Homo.

Sentinel cells, symbiotic bacteria and toxin resistance in the social amoeba Dictyostelium discoideum.

The social amoeba Dictyostelium discoideum is unusual among eukaryotes in having both unicellular and multicellular stages. In the multicellular stage, some cells, called sentinels, ingest toxins, waste and bacteria. The sentinel cells ultimately fall away from the back of the migrating slug, thus removing these substances from the slug. However, some D. discoideum clones (called farmers) carry commensal bacteria through the multicellular stage, while others (called non-farmers) do not. Farmers profit from their beneficial bacteria. To prevent the loss of these bacteria, we hypothesize that sentinel cell numbers may be reduced in farmers, and thus farmers may have a diminished capacity to respond to pathogenic bacteria or toxins. In support, we found that farmers have fewer sentinel cells compared with non-farmers. However, farmers produced no fewer viable spores when challenged with a toxin. These results are consistent with the beneficial bacteria Burkholderia providing protection against toxins. The farmers did not vary in spore production with and without a toxin challenge the way the non-farmers did, which suggests the costs of Burkholderia may be fixed while sentinel cells may be inducible. Therefore, the costs for non-farmers are only paid in the presence of the toxin. When the farmers were cured of their symbiotic bacteria with antibiotics, they behaved just like non-farmers in response to a toxin challenge. Thus, the advantages farmers gain from carrying bacteria include not just food and protection against competitors, but also protection against toxins.