The African coelacanth genome provides insights into tetrapod evolution

Abstract

The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution. Genome sequencing and phylogenomic analysis show that the lungfish, not the coelacanth, is the closest living relative of tetrapods, that coelacanth protein-coding genes are more slowly evolving than those of tetrapods and lungfish, and that the genes and regulatory elements that underwent changes during the vertebrate transition to land reflect adaptation to a new environment. The African coelacanth (Latimeria chalumnae) attracted international attention when a specimen was netted off the South African coast in 1938, as coelacanths were thought to have gone extinct 70 million years ago. Now its genome has been sequenced. Phylogenomic analysis resolves the long-standing question of which lobe-finned fish is the closest living relative of the land vertebrates — it is the lungfish, and not the coelacanth. The protein-coding genes of the coelacanth are slowly evolving, which perhaps explains how similar today's coelacanth looks to its 300-million-year-old fossil ancestors. Examination of changes in genes and regulatory elements shows the importance of factors including brain and fin development, immunity and nitrogen excretion in the adaptation of vertebrates to land.