Evolved increases in hemoglobin-oxygen affinity and Bohr effect coincided with the aquatic specialization of penguins

Abstract

AbstractDive capacities of air-breathing vertebrates are dictated by onboard O2stores, suggesting that physiological specializations of diving birds like penguins may have involved adaptive changes in convective O2transport. It has been hypothesized that increased hemoglobin (Hb)-O2affinity improves pulmonary O2extraction and enhance capacities for breath-hold diving. To investigate evolved changes in Hb function associated with the aquatic specialization of penguins, we integrated comparative measurements of whole-blood and purified native Hbs with protein engineering experiments based on site-directed mutagenesis. We reconstructed and resurrected ancestral Hbs representing the common ancestor of penguins and the more ancient ancestor shared by penguins and their closest nondiving relatives (order Procellariiformes, which includes albatrosses, shearwaters, petrels, and storm petrels). These two ancestors bracket the phylogenetic interval in which penguin-specific changes in Hb function would have evolved. The experiments revealed that penguins evolved a derived increase in Hb-O2affinity and a greatly augmented Bohr effect (reduced Hb-O2affinity at low pH). Although an increased Hb-O2affinity reduces the gradient for O2diffusion from systemic capillaries to metabolizing cells, this can be compensated by a concomitant enhancement of the Bohr effect, thereby promoting O2unloading in acidified tissues. We suggest that the evolved increase in Hb-O2affinity in combination with the augmented Bohr effect maximizes both O2extraction from the lungs and O2unloading from the blood, allowing penguins to fully utilize their onboard O2stores and maximize underwater foraging time.