The Life History of Domesticated Genes Illuminates the Evolution of Novel Mammalian Genes

Abstract

Molecular domestications of transposable elements have occurred repeatedly during the evolution of eukaryotes. Mammals possess numerous single copy domesticated genes that have originated from the intronless multicopy transposable elements. The genesis and regulatory wiring of the Metaviridae-derived domesticated genes have been explained through phylogenomic analysis of more than 90 chordate genomes. Phylogenomic analysis has demonstrated that major diversification of these domesticated genes occurred in the ancestor of placental mammals. Mammalian domesticated genes have originated in several steps by independent domestication events. The analysis of active Metaviridae lineages in amniotes has demonstrated that domesticated genes originated from retroelement remains. The analysis of syntenic loci has shown that diverse domesticated genes and their chromosomal positions were fully established in the ancestor of placental mammals. During the domestication process, de novo acquisition of regulatory regions was crucial for the survival of the novel domesticated genes. The origin and evolution of de novo acquired promoters and untranslated regions in diverse mammalian domesticated genes have been explained by comparative analysis of orthologous gene loci. The origin of placental mammal-specific innovations and adaptations, such as placenta and newly evolved brain functions, was most probably connected to the regulatory wiring of domesticated genes and their rapid fixation in the ancestor of placental mammals.