Animal life is intimately associated with the ability to move, which allows animals to find food, reproduce or escape predators. Animal locomotion thereby relies on striated skeletal muscles, whose ultrastructure is strikingly similar even in non-related taxonomic groups such as cnidarians (a group of animals including jelly fish) and bilaterians (animals with fronts, backs, tops and bottoms, including all insects and vertebrates). It was this similarity that suggested a common evolutionary origin of striated skeletal muscles, albeit the molecular details of striated muscle evolution have not hitherto been addressed. In a phylogenetic study published recently in Nature, Ulrich Technau from the University of Vienna, Austria, and colleagues from various institutions around the world provided evidence for a convergent evolution model of striated muscles, in which newly evolved proteins were added progressively to ancient components of the contractile units promoting independent muscle evolution in cnidarian and bilaterian species.
Striated muscles are made of specialized cells that have fused to form contractile fibrils. These cells contain sequences of sarcomers, which are the smallest contractile units found in muscles. The sarcomers contain thin actin filaments and thick myosin-based filaments that slide against each other in an ATP-dependent manner resulting in contractions, which are meticulously regulated by additional muscle proteins such as the troponin complex. To reassess muscle evolution, the scientists defined a core set of muscle proteins and screened for their presence in various genomes. One of the core proteins that they focused on was a type II myosin heavy chain (MyHC) motor protein that emanated from a gene duplication event giving rise to two different phylogenetic forms: a striated muscle-specific form (ST MyHC) that functions in muscle contraction, and a non-muscle form (NM MyHC) that serves other cellular functions such as cell division or migration. Technau and his team expected that the gene duplication event that led to the appearance of ST MyHC would coincide with the emergence of striated muscles during the evolution of metazoan animals. To their big surprise, however, they found that ST MyHC was already present in unicellular organisms before the origin of muscles and multicellular animals.
Thrilled by this finding, they analysed the gene expression patterns for ST and NM MyHCs in different non-bilaterian sponges and cnidarians by whole-mount in situ hybridization. In muscle-lacking sponges, they found NM MyHC was expressed in a wide range of cells, whereas expression of ST MyHC was restricted to cells involved in controlling the water flow necessary for nutrition. The differential expression suggests that the diversification of ST and NM MyHC forms had already occurred before the emergence of striated muscles. Cnidarians, which possess striated muscles, express the ancient ST MyHC in muscle cells but they lack other components (such as the troponin complex, paramyosin or titin) that are typically found in striated muscles of ‘higher’ bilaterian animals. This finding in turn suggests that despite the striking ultrastructural similarities, striated muscles have evolved independently in cnidarian and bilaterian animals.
Ulrich Technau and his team showed that the origin of core components of striated muscle cells (such as ST MyHC) predates that of muscle cells, and that other components were added progressively during muscle evolution in different animal groups. The proposed convergent model of striated muscle evolution may also apply to the evolution of other specialized cell types, which also exhibit ultrastructural similarities in different animal groups.