The Impact of Hemoglobin Expression on Cardiovascular Physiology and Thermal Tolerance of Antarctic Notothenioid Fishes

Antarctic fishes from the suborder Notothenioidei provide excellent opportunities to investigate evolutionary adaptations to chronically cold body temperature. One family within the group, Channichthyidae, has the unique feature of lacking completely the oxygen-binding protein, hemoglobin (Hb). These animals have compensated for absence of an oxygen carrier with a suite of cardiovascular modifications: large hearts with numerous mitochondria, large blood volumes pumped through large diameter vessels, and high cardiac outputs. This study examines a number of questions related to the cardiovascular physiology and biochemistry of channichthyids, or 'icefishes,' using a variety of methodologies that include techniques from those used on the whole animal to others at the molecular level. I examined mechanistic underpinnings driving formation of one of the unusual traits we see in icefishes today, a remarkably dense vasculature within their eyes compared to those of red-blooded notothenioids. Results indicate that a biochemical pathway, nitric oxide-mediated angiogenesis, is patent in notothenioid fishes and may have led to the remarkable pattern of blood vessels in eyes of icefishes. I also found that mitochondrial populations within eyes of icefishes are particularly dense compared to those in Hb-expressing notothenioids. High densities of mitochondria provide a lipid-rich membranous network that aids diffusive flux of oxygen in species having reduced oxygen-carrying capacity because of the absence of a circulating oxygen carrier in their blood. Finally, organismal temperature sensitivities of notothenioid fishes reveal that the pattern of Hb expression in notothenioids influences thermal tolerance limits. Icefishes, in particular, are susceptible to acute elevations of temperature and my results support the hypothesis that oxygen may be the limiting factor in setting their maximum thermal limits. Thus, hemoglobinless icefishes may be a sentinel taxon for climatic warming in the Antarctic region. This research provides insights into several different physiological/biochemical processes that are fundamental to vertebrate animals and may have important applications to both biomedicine and problems associated with global climate change.