Repeated evolutionary turnover of vertebrate skeletal muscle myosins

Abstract

Myosin heavy chain proteins are essential for muscle contraction and nearly every physiological function in animals, but their diversity and evolution outside mammals is largely unknown. We comprehensively model the evolutionary history of over 1100 heavy-chain myosins. We find that skeletal muscle myosins are located in a conserved tandem gene array in all vertebrate species, but repeated gene duplication-loss turnover has surprisingly led to an independently evolved set of core skeletal muscle myosins in each major vertebrate group. Despite these separate derivations of these myosin subfamilies, each major vertebrate group exhibits consistent tissue-specific patterns of subfamily expression and specialized myosin subfamily expression in extreme muscles. Our results show that muscle evolution across vertebrates is not based in conserved orthologous motor myosins, as might be expected for such a core structural protein family. Instead, we find that skeletal muscle myosins have evolved as a shifting cluster of genes that is constantly changing and diversifying to balance the need to maintain core physiology, while innovating new physiological possibilities.