Genomic basis of evolutionary adaptation in a warm-blooded fish

Abstract

Few fishes have evolved elevated body temperatures compared with ambient temperatures, and only in opah (Lampris spp) is the entire body affected. To understand the molecular basis of endothermy, we analyzed the opah genome and identified 23 genes with convergent amino acid substitutions across fish, birds, and mammals, including slc8b1, which encodes the mitochondrial Na+/Ca2+ exchanger and is essential for heart function and metabolic heat production. Among endothermic fishes, 44 convergent genes with suggestive metabolic functions were identified, such as glrx3, encoding a crucial protein for hemoglobin maturation. Numerous genes involved in the production and retention of metabolic heat were also found to be under positive selection. Analyses of opah's unique inner-heat-producing pectoral muscle layer (PMI), an evolutionary key innovation, revealed that many proteins were co-opted from dorsal swimming muscles for thermogenesis and oxidative phosphorylation. Thus, the opah genome provides valuable resources and opportunities to uncover the genetic basis of thermal adaptations in fish. Public summary: • Endothermy has evolved multiple times in fishes (teleosts and chondrichthyans) • Opah genome explaining genetic changes in heat production and the sensory and immune system • Convergent evolution of genes in endothermic vertebrate lineages was investigated • Analyses of the pectoral muscle of opah revealed numerous highly expressed genes for thermogenesis

Keywords

• endothermy
• opah
• whole-genome sequencing
• convergent evolution
• thermogenesis