Gene Expression Divergence Recapitulates the Developmental hourglass model

Nature 468, 811-814; doi:10.1038/nature09634

Abstract:

The observation that animal morphology tends to be conserved during the embryonic phylotypic period(a period of maximal similarity between the species within each animal phylum) led to the proposition that embryogenesis diverges more extensively early and late than in the middle, known as the hourglass model. This patter of conservation is though to reflect a major constraint on the evolution of animal body plans. Despite a wealth of morphological data confirming that there is often remarkable divergence in the early and late embryos of species from the same phylum, it is not yet known to what extent gene expression evolution , which has a central role in the elaboration of different animal forms, underpins the morphological  hourglass pattern. Here we address this question using species  specific microarrays designed from six sequenced Drosophila species separated by up to 40 million years. We quantify divergence at different times during embryogenesis and show that expression is maximally conserved during the arthropod phylotypic period. By fitting different evolutionary models to each gene, we show that at each time point more than 80% of gene fit best to models incorporating stabilizing selection and that for genes whose evolutionarily optimal expression level is the same across all species, selective constraint is maximized during the phylotypic period. The genes that conform most to the hourglass pattern are involved in key developmental processes. These results indicate that natural selection acts to conserve patterns of gene expression during mid embryogenesis and provide a genome wide insight into the molecular basis of the hourglass pattern of developmental evolution.