Evolutionary transition in accessible chromatin landscapes during vertebrate embryogenesis

Abstract

The relationship between development and evolution is a central topic in evolutionary biology1,2. Recent transcriptome-based studies support the developmental hourglass model, which predicts that the animal embryogenetic program is most strongly conserved at mid-embryonic stages3-9. This model does not necessarily contradict the classical hypothesis10,11 that animal development recapitulates its evolutionary history after the mid-embryonic stages2,12. However, to date there is no molecular evidence supporting the hypothesis that gene-expression profiles that are more evolutionarily derived appear sequentially in late development. Here, by estimating activated genomic regions and their evolutionary origins, we show that the recapitulative pattern appears during late embryonic stages. We made a genome-wide assessment of accessible chromatin regions throughout embryogenesis in three vertebrate species (mouse, chicken, and medaka) and determined the phylogenetic range at which these regions were shared. In all three species, sequential activation of putative regulatory regions that were more derived occurred later in embryogenesis, whereas ancestral ones tended to be activated early. Our results clarify the chronologic changes in accessible chromatin landscapes and reveal a phylogenetic hierarchy in the evolutionary origins of putative regulatory regions that parallels developmental stages of activation. This relationship may explain, at least in part, the background for morphological observations of recapitulative events during embryogenesis.