The hourglass model of evolutionary conservation during embryogenesis extends to developmental enhancers with signatures of positive selection

Abstract

Inter-species comparisons of both morphology and gene expression within a phylum have revealed a period in the middle of embryogenesis with more similarity between species compared to earlier and later time-points. This developmental hourglass pattern has been observed in many phyla, yet the evolutionary constraints on gene expression, and underlying mechanisms of how this is regulated, remains elusive. Moreover, the role of positive selection on gene regulation in the more diverged earlier and later stages of embryogenesis remains unknown. Here, using DNase-seq to identify regulatory regions in two distant Drosophila species (D. melanogaster and D. virilis), we assessed the evolutionary conservation and adaptive evolution of enhancers throughout multiple stages of embryogenesis. This revealed a higher proportion of conserved enhancers at the phylotypic period, providing a regulatory basis for the hourglass expression pattern. Using an in silico mutagenesis approach, we detect signatures of positive selection on developmental enhancers at early and late stages of embryogenesis, with a depletion at the phylotypic period, suggesting positive selection as one evolutionary mechanism underlying the hourglass pattern of animal evolution.

Somatic embryogenesis of grapevine (Vitis vinifera) expresses a transcriptomic hourglass

“…al. 2017) and positive selection acting on the early and late phases of embryogenesis (Liu et al 2021) shape the hourglass profile in animals. Similar studies in plants are currently lacking; however, there is a possibility that evolutionary mechanisms behind developmental hourglass in plants are more complex than in animals.…”

Cis -regulatory landscapes in the evolution and development of the mammalian skull

“…As a consequence of such changes, many aspects of morphogenesis can be modulated, such as anisotropic proliferation rates, spatial distribution of proliferative zones and regions, qualitative and The hourglass model was originally proposed based on the observations that in the early and late embryonic stages, there is increased morphological divergence, while at the mid-embryonic stage-referred to as phylotypic period-the embryos within each animal phylum are morphologically similar. The conservation and divergence of genes, expression programmes and cis-elements also follow this pattern during embryonic development [119][120][121]. Deep conservation and low divergence of the mid-embryonic period is considered a source of the basic body plan formation, thus the active enhancers at this defined period are mostly associated with essential developmental genes that control patterning.…”

Heart Enhancers: Development and Disease Control at a Distance

“…Overall, the discordance between sequence and functional conservation may account for a significant portion of the weakly conserved heart enhancers. Second, an increasing number of studies indicate that the conservation of enhancers active in early embryonic development follows an hour-glass like pattern (Bogdanovic et al, 2012;Bogdanović et al, 2016;Liu et al, 2020) similar to that of transcriptomes (Irie and Sehara-Fujisawa, 2007;Domazet-Lošo and Tautz, 2010;Kalinka et al, 2010;Irie and Kuratani, 2011;Yanai et al, 2011). However, much less is known about "phylotypic enhancers" that presumably are established prior to organogenesis to set up conserved vertebrate gene expression patterns.…”