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

Abstract

Dive capacities of air-breathing vertebrates are dictated by onboard O2 stores, suggesting that physiologic specialization of diving birds such as penguins may have involved adaptive changes in convective O2 transport. It has been hypothesized that increased hemoglobin (Hb)-O2 affinity improves pulmonary O2 extraction and enhances the capacity 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 Hb with protein engineering experiments based on site-directed mutagenesis. We reconstructed and resurrected ancestral Hb 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-O2 affinity and a greatly augmented Bohr effect (i.e., reduced Hb-O2 affinity at low pH). Although an increased Hb-O2 affinity reduces the gradient for O2 diffusion from systemic capillaries to metabolizing cells, this can be compensated by a concomitant enhancement of the Bohr effect, thereby promoting O2 unloading in acidified tissues. We suggest that the evolved increase in Hb-O2 affinity in combination with the augmented Bohr effect maximizes both O2 extraction from the lungs and O2 unloading from the blood, allowing penguins to fully utilize their onboard O2 stores and maximize underwater foraging time.

Genomic insights into the secondary aquatic transition of penguins

“…18 ) show penguin-specific amino acid substitutions that are highly conserved across all penguin species, making them candidate molecular adaptations for surviving deep oceanic dives under hypoxic conditions (see also ref. 37 ). MB is an oxygen-binding myoglobin gene that shows positive selection at multiple sites both between penguins and other birds and among penguins (Fig.…”

Blood oxygen transport and depletion in diving emperor penguins

“…Temperature correction of the dissociation curve of emperor penguins was not possible because, although arterial and vena caval temperatures increase slightly during dives of penguins at the isolated dive hole ( Ponganis et al, 2001 , 2004 , 2003 ), the temperature sensitivity of their O 2 –Hb dissociation curve is not known. As recently reviewed for the Bohr shift in penguins ( Meir and Ponganis, 2009 ; Signore et al, 2021 ) and for increased temperature in high-flying geese ( Meir and Milsom, 2013 ), we expect that a decrease in pH or an increase in temperature would decrease Hb's affinity for O 2 during longer dives, enhancing O 2 delivery to tissues and lowering venous Hb saturation. However, that does not affect our interpretation of blood flow patterns from Hb saturation profiles during dives.…”

Evolution of an extreme hemoglobin phenotype contributed to the sub-Arctic specialization of extinct Steller’s sea cows

“…Given both the marked functional changes observed for H. gigas Hb and the correspondingly large ecological and thermal shifts encountered by ancestral hydrodamaline sea cows following their exploitation of the North Pacific in the Miocene ( Heritage and Seiffert, 2022 ), it is surprising that previous work failed to provide evidence for positive selection or an accelerated amino acid substitution rate for any globin loci in the Steller’s sea cow branch ( Signore et al, 2019 ). However, this result is not unique to hydrodamalines, as the Hb coding genes of woolly mammoths and stem penguins also lack statistically significant signatures of positive selection accompanying their niche transitions despite clear directional changes in their Hb properties ( Campbell et al, 2010a ; Signore et al, 2021 ).…”