ArticlePLoS genetics2013
The hourglass and the early conservation models--co-existing patterns of developmental constraints in vertebrates.
Article in PLoS genetics, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 36 papers.
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Who cites it
36 citing papers in PubMed.
- Developmental contexts of gene-regulatory evolution following whole genome duplication in salmonids.Nature ecology & evolution · 2026Article
- Molting in Pancrustacea Is Characterized by Both Deeply Conserved and Recently Evolved Gene Modules.Genome biology and evolution · 2026Article
- A cellular basis for the hourglass pattern in vertebrate embryogenesis.Nature communications · 2026Review
- The Interplay of Ontogeny and Phylogeny at the Transcriptome Level of the Tetrapod Heart.Journal of experimental zoology. Part B, Molecular and developmental evolution · 2025Article
- Codon Usage Bias: A Potential Factor Affecting VGLUT Developmental Expression and Protein Evolution.Molecular neurobiology · 2025Article
- A transcriptomic hourglass in brown algae.Nature · 2024Article
- Evolutionary mechanisms modulating the mammalian skull development.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2023Review
- Evolutionary Morphogenesis of Sexual Fruiting Bodies in Basidiomycota: Toward a New Evo-Devo Synthesis.Microbiology and molecular biology reviews : MMBR · 2022Review
- Article
- Molecular Evolution across Mouse Spermatogenesis.Molecular biology and evolution · 2022Article
- The new chimeric chiron genes evolved essential roles in zebrafish embryonic development by regulating NADScience China. Life sciences · 2021Article
- Article
- Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo.BMC biology · 2020Article
- Developmental transcriptomes of the sea star, Patiria miniata, illuminate how gene expression changes with evolutionary distance.Scientific reports · 2019Article
- Molecular evolution across developmental time reveals rapid divergence in early embryogenesis.Evolution letters · 2019Article
- Adaptation and Conservation throughout the Drosophila melanogaster Life-Cycle.Genome biology and evolution · 2019Article
- Adaptive Evolution of Animal Proteins over Development: Support for the Darwin Selection Opportunity Hypothesis of Evo-Devo.Molecular biology and evolution · 2018Article
- Developmental Constraints on Genome Evolution in Four Bilaterian Model Species.Genome biology and evolution · 2018Article
- Article
- Transcriptomic signatures shaped by cell proportions shed light on comparative developmental biology.Genome biology · 2017Article
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5 authors.
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No grant is acknowledged in the PubMed record.
Abstract
Developmental constraints have been postulated to limit the space of feasible phenotypes and thus shape animal evolution. These constraints have been suggested to be the strongest during either early or mid-embryogenesis, which corresponds to the early conservation model or the hourglass model, respectively. Conflicting results have been reported, but in recent studies of animal transcriptomes the hourglass model has been favored. Studies usually report descriptive statistics calculated for all genes over all developmental time points. This introduces dependencies between the sets of compared genes and may lead to biased results. Here we overcome this problem using an alternative modular analysis. We used the Iterative Signature Algorithm to identify distinct modules of genes co-expressed specifically in consecutive stages of zebrafish development. We then performed a detailed comparison of several gene properties between modules, allowing for a less biased and more powerful analysis. Notably, our analysis corroborated the hourglass pattern at the regulatory level, with sequences of regulatory regions being most conserved for genes expressed in mid-development but not at the level of gene sequence, age, or expression, in contrast to some previous studies. The early conservation model was supported with gene duplication and birth that were the most rare for genes expressed in early development. Finally, for all gene properties, we observed the least conservation for genes expressed in late development or adult, consistent with both models. Overall, with the modular approach, we showed that different levels of molecular evolution follow different patterns of developmental constraints. Thus both models are valid, but with respect to different genomic features.
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