Gene expression divergence recapitulates the developmental hourglass model

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 pattern of conservation is thought 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 genes 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.

Comparative transcriptomics across 14 Drosophila species reveals signatures of longevity

“…We found that the phylogenetic signals were low for many genes (Figure S3d; median values: λ = 0.03, K  = 0.41), suggesting most of the variations observed were not fully accounted for by the BM model. In addition, when we compared the goodness of fit of individual gene expression under BM model against OU models with up to three optima (Butler & King, 2004; Kalinka et al., 2010), we found over 85% of the genes fitted better with one of the OU models than with the BM model (Figure S3e,f), similar to the percentage previously observed (Kalinka et al., 2010). Together, these data suggest that stabilizing selection likely plays an important role in influencing the gene expression patterns in Drosophila .…”

“…On the other hand, previous studies based on genomes and transcriptomes observed that a large fraction of the genes in Drosophila were likely subjected to stabilizing selection (Bedford & Hartl, 2009; Clark et al., 2007; Kalinka et al., 2010; Rifkin, Kim & White, 2003), such that the increase in gene expression divergence eventually reaches a plateau (Bedford & Hartl, 2009) and may be better described by Ornstein‐Uhlenbeck (OU) process (Butler & King, 2004; Martins & Hansen, 1997). …”

Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification

“…Genes for which we observe no change in H3K27me3 signal may instead be highly diverged at other developmental times. Furthermore, it is possible that the dynamics of histone modification evolution differ depending on the stage of development (Kalinka et al 2010). Additionally, we believe the observed differences in H3K27me3 reflect a lower bound estimate of the possible differences between species.…”

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

“…Indeed, TFs play a crucial role in multicellular eukaryotes. For example, TFs are the master regulators of embryonic development in embryophytes and metazoans (9), and analyses of their embryonic transcriptional profiles support the presence of a phylotypic stage in both lineages (10)(11)(12)(13)(14). These studies have also shown that evolutionarily younger genes tend to be expressed at earlier and later stages of development, whereas the transcriptomes of the middle stages (the phylotypic stage) are dominated by ancient genes (10,13).…”