Phylotranscriptomic investigation into the evolution of endothermy in fish

Adam Guy Ciezarek, Vincent Savolainen, British Biological Science Research Council
2019
Regional endothermy, where metabolically-derived heat is used to maintain elevated temperatures in parts of the body, has independently evolved in several lineages of pelagic, predatory fish, including billfish, tuna, lamnid sharks and the opah. The lamnid sharks and tunas demonstrate a striking phenotypic convergence, despite 450 million years of independent evolution. This is characterised by a distinctive muscle morphology, which has enabled them to utilise a unique stiff-bodied swimming
more » ... e and maintain elevated muscular temperatures and metabolic capacities. This has facilitated expansions in thermal niche and increases in swimming speed and exercise recovery rate. We find selection has acted on one gene independently in both groups, glycogenin-1, which is associated with post-exercise glycogen replenishment. Different metabolic pathways have been targeted by selection in either group. Amongst the endothermic fish, there is considerable variability between species in endothermic capacity and cold-tolerance. By investigating diversification among the eight Thunnus tuna species, we find that the three highly cold-tolerant and endothermic bluefin tuna species are paraphyletic. We infer that parallel selection on ancestral genetic variation is likely to have enabled their evolution. This includes selection for variants in genes associated with metabolism and thermogenesis in other animals. Adaptations in the cardiac system of bluefin tuna are crucial to their ability to tolerate cold-water, as their heart operates at ambient temperature yet must supply oxygen for metabolically demanding warm muscle. We show that this elevated cardiac capacity is associated with increased expression of a key sarcoplasmic reticulum calcium-cycling gene, SERCA2b, in the atrium. Tuna muscle has a thermal gradient, with temperatures highest in the centre of the body. We found no upregulation of metabolic or thermogenesis genes in regions of warm muscle, indicating that intrinsic muscular contraction is sufficient for heat productio [...]
doi:10.25560/73282 fatcat:hgghlgxn7nam7jkjvqwjdqijlq