Parallel embryonic transcriptional programs evolve under distinct constraints and may enable morphological conservation amidst adaptation

Abstract

Embryonic development evolves by balancing stringent morphological constraints with genetic and environmental variation. The design principle that allows developmental transcriptional programs to conserve embryonic morphology while adapting to environmental changes is still not fully understood. To address this fundamental challenge, we compare developmental transcriptomes of two sea urchin species, Paracentrotus lividus and Strongylocentrotus purpuratus, that shared a common ancestor about 40 million years ago and are geographically distant yet show similar morphology. We find that both developmental and housekeeping genes show highly dynamic and strongly conserved temporal expression patterns. The expression of other gene sets, including homeostasis and response genes, show divergent expression which could result from either evolutionary drift or adaptation to local environmental conditions. The interspecies correlations of developmental gene expressions are highest between morphologically similar developmental time points whereas the interspecies correlations of housekeeping gene expression are high between all the late zygotic time points. Relatedly, the position of the phylotypic stage varies between these two groups of genes: developmental gene expression shows highest conservation at mid-developmental stage, in agreement with the hourglass model while the conservation of housekeeping genes keeps increasing with developmental time. When all genes are combined, the relationship between conservation of gene expression and morphological similarity is partially masked by housekeeping genes and genes with diverged expression. Our study illustrates various transcriptional programs that coexist in the developing embryo and evolve under different constraints. Apparently, morphological constraints underlie the conservation of developmental gene expression while embryonic fitness requires the conservation of housekeeping gene expression and the species-specific adjustments of homeostasis gene expression. The distinct evolutionary forces acting on these transcriptional programs enable the conservation of similar body plans while allowing adaption.

Developmental transcriptomes of the sea star, Patiria miniata, illuminate the relationship between conservation of gene expression and morphological conservation

“…The interspecies correlations of the expression levels of developmental genes are high between morphologically similar stages in the two sea urchins, and decrease sharply between diverse developmental stages, resulting with highly diagonal correlation matrices [17]. The correlations peak at mid-development, at the onset of gastrulation, in agreement with the hourglass model of developmental conservation [17–19].…”

“…Time point 6hpf in S. purpuratus does not have RNA-seq data. (C) Relative gene expression in the three species measured in the current paper by RNA-seq for P. miniata (orange curves), in [17] by RNA-seq for P. lividus (purple curves) and in [23] by nanostring for S. purpuratus (black curves). Error bars indicate standard deviation.…”

“…Insight on the genome-wide changes in developmental gene expression can be gained from comparative transcriptome studies of related species at equivalent developmental stages [14–17]. We previously investigated different aspects of interspecies conservation of gene expression between P. lividus and the pacific sea urchin, Strongylocentrotus purpuratus ( S. purpuratus ) [16, 17]. These species diverged from their common ancestor about 40 million years ago and have a highly similar embryonic morphology (Fig.…”

“…1A). We observed high conservation of gene expression dynamics of both developmental genes (expressed differentially and regulate specific embryonic lineages) and housekeeping genes (expressed in all the cells throughout developmental time) [17]. Yet, the interspecies correlations of the expression levels of these two sets of genes show distinct behaviors.…”

“…The interspecies correlations of the expression levels of developmental genes are high between morphologically similar stages in the two sea urchins, and decrease sharply between diverse developmental stages, resulting with highly diagonal correlation matrices [17]. The correlations peak at mid-development, at the onset of gastrulation, in agreement with the hourglass model of developmental conservation [17–19]. Conversely, the interspecies correlations of housekeeping gene expression increase with developmental time and are high between all post-hatching time points, resulting with distinct off-diagonal elements of the correlation matrix [17].…”