Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
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RESEARCH ARTICLE
Open Access
Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo Jialin Liu1,2*, Michael Frochaux2,3, Vincent Gardeux2,3, Bart Deplancke2,3 and Marc Robinson-Rechavi1,2*
Abstract Background: The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass pattern have focused on purifying the selection of gene regulation. Here, we propose an alternative—genes are regulated in different ways at different stages and have different intrinsic capacities to respond to perturbations on gene expression. Results: To eliminate the influence of natural selection, we quantified the expression variability of isogenetic single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that the expression variability is lower at the phylotypic stage, supporting that the underlying regulatory architecture in this stage is more robust to stochastic variation on gene expression. We present evidence that the phylotypic stage is also robust to genetic variations on gene expression. Moreover, chromatin regulation appears to play a key role in the variation and evolution of gene expression. Conclusions: We suggest that a phylum-level pattern of embryonic conservation can be explained by the intrinsic difference of gene regulatory mechanisms in different stages. Keywords: Expression variability, Hourglass, Evo-devo
Background Both morphological and transcriptomic surveys have proposed an “hourglass” model of evo-devo [1, 2]. The mid-development phylotypic stage is more conserved than both early and late development [3–7]. Currently, the proposed mechanisms for this pattern are mainly based on how natural selection shapes the outcome of regulatory variation on gene expression. The first hypothesis interpreted high conservation as a result of negative selection [1, 2, 8]. For example, Raff suggested a high inter-dependence in signaling among developmental modules in middle development, so expression * Correspondence: [email protected]; [email protected] 1 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland Full list of author information is available at the end of the article
changes underlying this stage will generally be deleterious and under negative selection. An alternative hypothesis, however, argues that high conservation can also be the result of variation being less visible to positive selection [9, 10]. In this scenario, embryonic development is more likely to evolve when ecological niches demand it. For example, variation in early development can result from adaptation to diverse ecological circumstances [11]. To distinguish the two hypotheses, Zalts and Yanai [6] compared the expression variation of 20 Caenorhabditis elegans mutation accumulation strains across embryonic developmen
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