Integrated adaptations of muscle structure and mitochondrial function to locomotion demands in teleost fishes

Abstract Teleost fishes display diverse swimming modes supported by functional specialization of skeletal muscle. However, the ultrastructural adaptations and molecular mechanisms regulating mitochondrial homeostasis in relation to divergent locomotion remain unclear. We compared muscle fiber composition, mitochondrial ultrastructure, and regulatory pathways in two teleosts with contrasting swimming strategies: the sustained swimmer Pseudocaranx dentex and the burst swimmer Paralichthys olivaceus. Histological analyses revealed a higher proportion of slow-twitch fibers in P. dentex whose slow-twitch muscle also exhibited greater mitochondrial density and size. Transcriptomic and protein analyses indicated predominant aerobic metabolism in slow-twitch fibers and anaerobic metabolism in fast-twitch fibers in both species. The Sirt1-PGC-1α-TFAM axis was upregulated in slow-twitch muscle, supporting enhanced mitochondrial biogenesis. P. dentex also showed stronger activation of mitochondrial fusion and fission regulators, whereas autophagy-related pathways showed no fiber-type differences. The structural and functional specialization of skeletal muscle in teleost fishes is tightly coupled with their locomotive strategies. Enhanced slow-twitch fiber abundance, mitochondrial biogenesis, and dynamic remodeling in P. dentex support sustained aerobic performance, whereas P. olivaceus exhibits a muscle profile suited to rapid anaerobic burst swimming. These findings provide a valuable comparative framework for understanding the evolutionary plasticity of skeletal muscle energetics and mitochondrial regulation across aquatic vertebrates.