Altered hemoglobin co-factor sensitivity does not underlie the evolution of derived fossorial specializations in the family Talpidae

Abstract

The high O affinity of European mole (Talpa europaea) blood is postulated to largely arise from the presence of two β-globin chain residues (β4 Ser and β5 Gly) that weaken the interaction of its hemoglobin (Hb) with the red cell organophosphate 2,3-diphosphoglycerate (DPG). This latter trait is generally accepted to be an 'adaptation to subterranean life', despite the fact that no data are available for more basal mole lineages that have no evolutionary history of fossoriality (i.e. the ambulatory, high-elevation shrew-like moles and the semi-aquatic desmans), and which may similarly benefit from an elevated blood O affinity. To test whether evolution of a low DPG sensitivity phenotype is linked to derived fossorial lifestyles or represents an ancestral trait for the family, we determined the globin gene sequences and measured the intrinsic O affinity and co-factor sensitivity of the major Hb component of the gracile shrew-like mole (Uropsilus gracilis) and the Pyrenean desman (Galemys pyrenaicus). Our results unequivocally demonstrate that the presence of β4 Ser and β5 Gly, together with a low DPG sensitivity Hb phenotype, predates the radiation of the family Talpidae, and hence did not evolve as a specific adaptation to fossorial life. By contrast, our comparative analyses suggest that variations in whole blood O affinity among members of this family predominantly arose from amino acid substitutions that increase or decrease the intrinsic O affinity of the protein.