Unknown,Transcriptomics,Genomics,Proteomics

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Hourglass

ABSTRACT: The observation that animal morphology tends to be conserved during the embryonic phylotypic period led to the proposition that embryogenesis diverges more extensively early and late than in the middle, known as the hourglass model. This pattern of conservation is thought to reflect a major constraint on the evolution of animal body plans. Despite a wealth of morphological data confirming that there is often remarkable divergence in the early and late embryos of species from the same phylum, it is not yet known to what extent gene expression evolution, which plays a central role in the elaboration of different animal forms, underpins the morphological hourglass. Here we address this question using species-specific microarrays designed from six sequenced Drosophila species. Although it is generally appreciated that gene expression divergence plays a key role in the evolution of morphological diversity, no studies to date have addressed the extent to which expression divergence underpins the hourglass pattern at the genome-wide level. We test the molecular basis of the hourglass model of developmental evolution using gene expression data from six Drosophila species with sequenced genomes (D. ananassae, D. melanogaster, D. persimilis, D. pseudoobscura, D. simulans, and D. virilis) thereby enabling unambiguous quantitative comparisons across orthologous genes for a set of species separated by up to 40 million years. Gene expression levels were measured for 3019 genes, known to be expressed during embryonic development from RNA in situ data, at 2 hour intervals for the majority of embryogenesis using a microarray time-course with three biological replicates per species and four species-specific probes per gene.

ORGANISM(S): Drosophila simulans

SUBMITTER: Pavel Tomancak

PROVIDER: E-MTAB-404 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Project description:Early embryogenesis is a unique developmental stage where genetic control of development is handed off from mother to zygote. Yet the contribution of this transition to the evolution of gene expression is poorly understood. Here we study two aspects of gene expression specific to early embryogenesis in Drosophila: sex-biased gene expression prior to the onset of canonical X chromosomal dosage compensation, and the contribution of maternally supplied mRNAs. We sequenced mRNAs from individual unfertilized eggs, precisely staged and sexed blastoderm embryos and compared levels between D. melanogaster, D. yakuba, D. pseudoobscura and D. virilis. First, we find that mRNA content is highly conserved for a given stage and that studies relying on pooled embryos may systematically overstate the degree of gene expression divergence. Unlike studies done on larvae and adults, where most species show a larger proportion of genes with male-biased expression, we find that transcripts in Drosophila embryos are largely female-biased in all species, likely due to incomplete dosage compensation prior to the activation of the canonical dosage compensation mechanism. The divergence of sex-biased gene expression across species is observed to be often due to a decrease of expression, the most drastic example of which is the overall reduction of male expression from the neo-X chromosome in D. pseudoobscura, leading to a pervasive female-bias on this chromosome. We see no evidence for a faster evolution of expression on the X chromosome in embryos (no “faster X” effect), unlike in adults and contrary to a previous study on pooled non-sexed embryos. Finally, we find that most genes are conserved in regard to their maternal or zygotic origin of transcription, and present evidence that differences in maternal contribution to the blastoderm transcript pool may be due to species-specific divergence of transcript degradation rates We sequenced mRNA from D. melanogaser, D. yakuba, D. pseudoobscura and D. virilis single unfertilized eggs (1 to 2 per species) and from both single female and male embryos (3 per sex per species).

Project description:Neural crest (NC) is a vertebrate-specific embryonic progenitor cell population at the basis of important vertebrate features such as the craniofacial skeleton and pigmentation patterns. Despite the wide-ranging variation of NC-derived traits across vertebrates, the contribution of NC to species diversification remains underexplored. Here, leveraging the adaptive diversity of African Great Lakes' cichlid species, we combined comparative transcriptomics and population genomics to investigate the evolution of the NC genetic program in the context of their morphological divergence. Our analysis revealed substantial differences in transcriptional landscapes across somitogenesis, an embryonic period coinciding with NC development and migration. This included dozens of genes with described functions in the vertebrate NC gene regulatory network, several of which showed signatures of positive selection. Among candidates showing between-species expression divergence, we focused on teleost-specific paralogs of the NC-specifier sox10 (sox10a and sox10b) as prime candidates to influence NC development. These genes, expressed in NC cells, displayed remarkable spatio-temporal variation in cichlids, suggesting their contribution to interspecific morphological differences, such as craniofacial structures and pigmentation. Finally, through CRISPR/Cas9 mutagenesis, we demonstrated the functional divergence between cichlid sox10 paralogs, with the acquisition of a novel skeletogenic function by sox10a. When compared with teleost models zebrafish and medaka, our findings reveal that sox10 duplication, although retained in most teleost lineages, had variable functional fates across their phylogeny. Altogether, our study suggests that NC-related processes—particularly those controlled by sox10s—are involved in generating morphological diversification between species and lays the groundwork for further investigations into the mechanisms underpinning vertebrate NC diversification.

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Hourglass

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