Molecular evolution across developmental time reveals rapid divergence in early embryogenesis

Abstract

AbstractOntogenetic 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 co-expression modules of the C. 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 (maternal provisioning), are non-randomly distributed in the genome, and correspond to a life stage especially prone to inviability in inter-species hybrids. These observations conflict with the “early conservation model” for the evolution of development, though expression-weighted sequence divergence analysis provides some support for the “hourglass model.” Genes in co-expression 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 co-expression 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.Impact SummaryThe development of an organism from a single-celled embryo to a reproductive adult depends on dynamic gene expression over developmental time, with natural selection capable of shaping the molecular evolution of those differentially-expressed genes in distinct ways. We quantitatively analyzed the dynamic transcriptome profiles across 30 timepoints in development for the nematode C. elegans. In addition to rapid evolution of adult-expressed genes with functional roles in sperm, we uncovered the unexpected result that the distinctive set of genes that evolve fastest are those with peak expression in young embryos, conflicting with some models of the evolution of development. The rapid molecular evolution of genes in early embryogenesis contrasts with the exceptional conservation of embryonic cell lineages between species, and corresponds to a developmental period that is especially sensitive to inviability in inter-species hybrid embryos. We propose that these predictable trends of molecular evolution for dynamically-expressed genes across development predispose particular life stages, early embryogenesis in particular, to hybrid dysfunction in the speciation process.