Muscle metabolism and growth in Antarctic fishes (suborder Notothenioidei): Evolution in a cold environment

Abstract

The radiation of notothenioid fishes (order Perciformes) in the Southern Ocean provides a model system for investigating evolution and adaptation to a low temperature environment. The Notothenioid fishes comprising eight families, 43 genera and 122 species dominate the fish fauna in Antarctica. The diversification of the clade probably began 15-20 million years ago after the formation of the Antarctic Polar Front. The radiation was, therefore, associated with climatic cooling down to the present day temperature of -1.86°C. Origins and Evolution of the Antarctic Biota Geological Society Special Publication No. 47, Geological Society of London. pp. 253-268). The success of the group has been closely linked with the evolution of glycopeptide and peptide antifreezes, which are amongst the most abundant proteins in blood and interstitial fluid. The radiation of the clade has been associated with disaptation (evolutionary loss of function) and recovery. For example, it is thought that the icefishes (Channichyidae) lost haemoglobin through a single mutational event leading to the deletion of the entire β-globin gene and the 5′ end of the linked α-globin gene, resulting in compensatory adaptations of the cardiovascular system. Phylogenetically based statistical methods also indicate a progressive and dramatic reduction in the number of skeletal muscle fibres (FNmax) at the end of the recruitment phase of growth in basal compared to derived families. The reduction in FN max is associated with a compensatory increase in the maximum fibre diameter, which can reach 100 μm in slow and 600 μm in fast muscle fibres. At -1 to 0°C, the oxygen consumption of isolated mitochondria per mg mitochondrial protein shows no evidence of up-regulation relative to mitochondria from temperate and tropical Perciform fishes. The mitochondria content of slow muscle fibres in Antarctic notothenioids is towards the upper end of the range reported for teleosts with similar lifestyles, reaching 50% in Channichthyids. High mitochondrial densities facilitate ATP production and oxygen diffusion through the membrane lipid compartment of the fibre. Modelling studies suggest that adequate oxygen flux in the large diameter muscle fibres of notothenioids is possible because of the reduced metabolic demand and enhanced solubility of oxygen associated with low temperature. At the whole animal level size-corrected resting metabolic rate fits on the same temperature relationship as for Perciformes from warmer climates. It seems likely that the additional energetic costs associated with antifreeze synthesis and high mitochondrial densities are compensated for by reductions in other energy requiring processes: a hypothesis that could be tested with detailed energy budget studies. One plausible candidate is a reduction in membrane leak pathways linked to the loss of muscle fibres, which would serve to minimise the cost of maintaining ionic gradients. © 2003 Elsevier Inc. All rights reserved.