One of the greatest milestones in the history of life is the evolution of fish into land-dwelling animals, with four limbs instead of fins. The transition to a terrestrial life required dramatic alterations in the animals' trunk musculature, to maintain posture and transmit forces to and from the limbs. In fish and higher vertebrates, the sequence of events that leads to the formation of differentiated skeletal muscle is initiated early in development. Muscle progenitor cells arise in the embryo within the somites, a series of paired segments on either side of the developing spinal cord. In amniotes (birds, reptiles and mammals), many muscle progenitor cells also originate from the lateral surface of the somites in specialised structures called the dermomyotomes, which fish lack. However, the early appearance of muscle precursors in both fish and amniotes requires signalling by a family of developmental control genes known as hedgehog. This similarity between muscle development in teleosts and terrestrial amniotes suggests that a common ancestral muscle developmental programme might have adapted to different ends during the evolution of tetrapods from teleosts. Intrigued by this question, Annalisa Grimaldi and collaborators from King's College London and the University of California decided to look at muscle development in the African clawed frog, Xenopus laevis, as they have many traits in common with fish and modern amniotes.
The team started by using antibody staining to search for different types of muscle fibres in Xenopus embryos, identifying two that are also present in fish: superficial slow muscle fibres with a large number of mitochondria and fast muscle fibres. Next, the team went on to characterise the differentiation pattern of the two muscle fibre types. Their results showed a remarkable difference between the tail somites, which are committed to cell death, and the trunk somites in the embryo's anterior region, which eventually will form most of the adult musculature. In trunk somites, the earliest formed muscle is fast. However, in tail somites, slow muscle precursors appear first and then migrate to the surface, as most of the somite differentiates into fast muscle. Later on in development, a second wave of slow fibres appears in all somites. Remarkably, the pattern observed in tail somites is reminiscent of that found throughout the whole body of fish. The team also found a thin layer of distinct cells around the surface of trunk and anterior tail somites, similar to that found in amniotes. These cells express the protein pax3, a dermomyotome marker, and hence, they are probably a homologue of the amniote dermomyotome. Next, the team began investigating the influence of hedgehog signalling in muscle development by overexpressing a transcription factor known as sonic hedgehog or blocking its expression in Xenopus embryos. They found that sonic hedgehog induces the formation of first wave but not second wave slow muscle fibres, just like in fish.
The similarities shared by Xenopus with both fish and amniotes during early muscle development provide new insight into the evolution of somite differentiation. It seems that muscle development in the common ancestor of teleosts and tetrapods occurred in a manner similar to that observed in Xenopus tail. The authors propose that the blocking of the normal hedgehog function in trunk somites allows muscle precursors to adopt fates other than first wave slow muscle; these cells can go on to form the dermomyotome, which generates much of the later muscle in tetrapods. Perhaps this evolutionary innovation was the key to the dramatic changes in trunk musculature that allowed our tetrapod ancestors, such as the crocodile-like creature Pederpes finneyae, to crawl out of the water and conquer the land some 350 million years ago.
- © The Company of Biologists Limited 2004