Molecular evolution across developmental time reveals rapid divergence in early embryogenesis

Abstract

Ontogenetic development hinges on the changes in gene expression in time and space within an organism, suggesting that the demands of ontogenetic growth can impose or reveal predictable pattern in the molecular evolution of genes expressed dynamically across development. Here, we characterize coexpression modules of the Caenorhabditis elegans transcriptome, using a time series of 30 points from early embryo to adult. By capturing the functional form of expression profiles with quantitative metrics, we find fastest evolution in the distinctive set of genes with transcript abundance that declines through development from a peak in young embryos. These genes are highly enriched for oogenic function and transient early zygotic expression, are nonrandomly distributed in the genome, and correspond to a life stage especially prone to inviability in interspecies hybrids. These observations conflict with the “early conservation model” for the evolution of development, although expression‐weighted sequence divergence analysis provides some support for the “hourglass model.” Genes in coexpression modules that peak toward adulthood also evolve fast, being hyper‐enriched for roles in spermatogenesis, implicating a history of sexual selection and relaxation of selection on sperm as key factors driving rapid change to ontogenetically distinguishable coexpression modules of genes. We propose that these predictable trends of molecular evolution for dynamically expressed genes across ontogeny predispose particular life stages, early embryogenesis in particular, to hybrid dysfunction in the speciation process.

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

“…The 96 genes in M21 have extremely consistent expression across replicates, with most showing no individually significant differential expression due to either temperature or genotype (Figures and c). In C. elegans , these features are typical of genes that are expressed constitutively across development (Cutter et al, ).…”

“…Overall, genes in operons were much less likely to show significant differential expression than nonoperon genes (43% of operon vs. 56% of nonoperon genes; Fisher's exact test, p < .0001). Caenorhabditis elegans operon genes, most of which are conserved in C. briggsae (Qian & Zhang, ), are known to show high expression during growth, as for gonad tissue (Reinke & Cutter, ) and following growth‐arrested states (Zaslaver, Baugh, & Sternberg Paul, ), and generally have nondynamic expression profiles across ontogeny (Cutter et al, ). These observations are consistent with operon genes being disproportionately robust to both environmental and genetic perturbations.…”

Evolutionary Dynamics of the SKN-1 → MED → END-1,3 Regulatory Gene Cascade inCaenorhabditisEndoderm Specification

“…Consistent with this, calculations of synonymous and non-synonymous substitutions rates did not produce interpretable information because of the high rates of molecular evolution in Caenorhabditis in general (Cutter 2008). Moreover, the fastest rates of evolution in Caenorhabditis occur in early zygotic regulators with transient expression, which accurately describes the MED and END factors (Cutter et al 2019). Because fast-evolving proteins are being compared among 20 species (as opposed to only two or three), the major conclusions regarding conserved amino acids and stringency of selection are nonetheless self-evident from the alignments and topology of phylogenetic trees.…”

Speciation and the developmental alarm clock

“…Cellular development in embryos is conserved across species, being nearly indistinguishable at least to the 350-cell stage (Zhao et al 2008, Memar et al 2018. In hybrid crosses of most species pairs, however, embryos arrest around gastrulation Yen 2000, Baird andSeibert 2013), near the time that expression divergence appears minimized across Caenorhabditis (Levin et al 2012) and that expressionweighted coding sequence divergence is lowest (Cutter et al 2019). Coding sequences with fastest molecular evolution show peak expression very early in embryogenesis or toward adulthood Ward 2005, Cutter et al 2019) (Box 3).…”