Recent Evolution of the Hemoglobinless Condition of the Antarctic Icefishes

Abstract

Certainly one of the most unusual “adaptations” of vertebrates is the loss of erythrocytes and the oxygen transport protein hemoglobin [[1]] by the Antarctic icefishes (family Channichthyidae, suborder Nototheniodei). Lacking an oxygen transporter, the icefishes nonetheless maintain normal metabolic function by delivering oxygen to their tissues in physical solution in their “colorless” or “white” blood. In the chronically cold (−1.86 to+1 C) and oxygen-rich environment experienced by these psychrophilic organisms, reduction of the hematocrit to near zero appears to have been selectively advantageous because it significantly diminishes the energetic cost associated with circulation of a highly viscous, corpuscular blood fluid [[2]–[5]]. Hematocrit, mean cellular hemoglobin concentration, and hemoglobin chain multiplicity all decrease with increasing phylogenetic divergence among the red-blooded Antarctic notothenioid fishes [[6]], and the Bathydraconidae (the sister group to the channichthyids) approach the hematological extreme displayed by the white-blooded icefishes. Nevertheless, the development in icefishes of compensatory physiological and circulatory adaptations that reduce tissue oxygen demand and enhance oxygen delivery (e.g., modest suppression of metabolic rates, enhanced gas exchange by large, well-perfused gills and a scaleless skin, and large increases in cardiac output and blood volume) argues that loss of hemoglobin and erythrocytes was probably maladaptive under conditions of physiological stress. Therefore, the most plausible evolutionary scenario is that the phylogenetic trend to reduced hematocrits and decreased hemoglobin synthesis in notothenioid fishes developed concurrently with enhancements to their respiratory and circulatory systems, leading ultimately to the acorpuscular, hemoglobinless condition of the icefishes.