Distinct and shared endothermic strategies in the heat producing tissues of tuna and other teleosts

Although most fishes are ectothermic, some, including tuna and billfish, achieve endothermy through specialized heat producing tissues that are modified muscles. How these heat producing tissues evolved, and whether they share convergent molecular mechanisms, remain unresolved. Here, we generated a high-quality genome from the mackerel tuna (Euthynnus affinis) and investigated the heat producing tissues of this fish by single-nucleus and bulk RNA sequencing. Compared with other teleosts, tuna-specific genetic variation is strongly associated with muscle differentiation. Single-nucleus RNA-seq revealed a high proportion of specific slow skeletal muscle cell subtypes in the heat producing tissues of tuna. Marker genes of this cell subtype are associated with the relative sliding of actin and myosin, suggesting that tuna endothermy is mainly based on shivering thermogenesis. In contrast, cross-species transcriptome analysis indicated that endothermy in billfish relies mainly on non-shivering thermogenesis. Nevertheless, the heat producing tissues of the different species do share some tissue-specific genes, including vascular-related and mitochondrial genes. Overall, although tunas and billfishes differ in their thermogenic strategies, they share similar expression patterns in some respects, highlighting the complexity of convergent evolution.