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.
10Understanding the plasticity, robustness, and modularity of transcriptome expression to genetic 11 and environmental conditions is crucial to deciphering how organisms adapt in nature. To test 12 how genome architecture influences transcriptome profiles, we quantified expression responses 13 for distinct temperature-adapted genotypes of the nematode Caenorhabditis briggsae when 14 exposed to chronic temperature stresses throughout development. We found that 56% of the 15 8795 differentially-expressed genes show genotype-specific changes in expression in response 16to temperature (genotype-by-environment interactions, GxE). Most genotype-specific responses 17 occur under heat stress, indicating that cold versus heat stress responses involve distinct 18 genomic architectures. The 22 co-expression modules that we identified differ in their 19 enrichment of genes with genetic versus environmental versus interaction effects, as well as 20 their genomic spatial distributions, functional attributes, and rates of molecular evolution at the 21 sequence level. Genes in modules enriched for simple effects of either genotype or temperature 22 alone tend to evolve especially rapidly, consistent with disproportionate influence of adaptation 23 or weaker constraint on these subsets of loci. Chromosome scale heterogeneity in nucleotide 24 polymorphism, however, rather than the scale of individual genes, predominate as the source of 25 genetic differences among expression profiles, and natural selection regimes are largely 26 decoupled between coding sequences and non-coding flanking sequences that contain cis-27 regulatory elements. These results illustrate how the form of transcriptome modularity and 28 genome structure contribute to predictable profiles of evolutionary change. 29 30
Fibrillin microfibrils are widely distributed components of extracellular matrices that function in the formation of elastin, serve structural roles and provide substrates for cell adhesion. To determine when and how fibrillin-1 (fib-1) may function in early development we have examined the temporal and spatial distribution of fib-1 in chicken embryos. Using homologous PCR we amplified and cloned a 407 nt fragment of chicken cDNA that appears to code for an orthologue of FBN-1. Bacterially expressed protein was used to prepare two monoclonal antibodies, both of which recognize a 350 kD band in immunoblots or immunoprecipitates in supernatants of chicken embryonic aorta cells or human MG-63 cells. Both antibodies recognize fibrillar material associated with the surfaces of cultured cells. The antibodies appear to be specific for fib- as there was only weak cross reactivity to a bacterially expressed fragment from the corresponding region of fib-2 and the pattern of immunofluorescence in embryonic tissue is distinctly different from that of JB-3, a fib-2 specific antibody (Rongish et al. 1998). In embryos, fib-1 is first detected at stage 6 in the epiblast during gastrulation. In subsequent stages fib-1 fibers appear in all tissues and are present throughout the first 6 days of development. Immunoreactive fibers are present in basal laminae and mesenchyme filled spaces, but they also form random arrays with an apical-basal polarity within epithelia. Using primers specific for FBN-1 and FBN-2 in RT-PCR reactions we confirm the presence of fib- 1 and fib-2 mRNA in early embryonic stages. This temporal and spatial distribution indicates fib-1 has functions in early development that are distinct from fib-2.
Understanding the plasticity, robustness and modularity of transcriptome expression to genetic and environmental conditions is crucial to deciphering how organisms adapt in nature. To test how genome architecture influences transcriptome profiles, we quantified expression responses for distinct temperature‐adapted genotypes of the nematode Caenorhabditis briggsae when exposed to chronic temperature stresses throughout development. We found that 56% of the 8,795 differentially expressed genes show genotype‐specific changes in expression in response to temperature (genotype‐by‐environment interactions, GxE). Most genotype‐specific responses occur under heat stress, indicating that cold vs. heat stress responses involve distinct genomic architectures. The 22 co‐expression modules that we identified differ in their enrichment of genes with genetic vs. environmental vs. interaction effects, as well as their genomic spatial distributions, functional attributes and rates of molecular evolution at the sequence level. Genes in modules enriched for simple effects of either genotype or temperature alone tend to evolve especially rapidly, consistent with disproportionate influence of adaptation or weaker constraint on these subsets of loci. Chromosome‐scale heterogeneity in nucleotide polymorphism, however, rather than the scale of individual genes predominates as the source of genetic differences among expression profiles, and natural selection regimes are largely decoupled between coding sequences and noncoding flanking sequences that contain cis‐regulatory elements. These results illustrate how the form of transcriptome modularity and genome structure contribute to predictable profiles of evolutionary change.
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 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 3 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.
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