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Gene expression divergence recapitulates the developmental hourglass model

Abstract

The observation that animal morphology tends to be conserved during the embryonic phylotypic period (a period of maximal similarity between the species within each animal phylum) led to the proposition that embryogenesis diverges more extensively early and late than in the middle, known as the hourglass model1,2. This pattern of conservation is thought to reflect a major constraint on the evolution of animal body plans3. Despite a wealth of morphological data confirming that there is often remarkable divergence in the early and late embryos of species from the same phylum4,5,6,7, it is not yet known to what extent gene expression evolution, which has a central role in the elaboration of different animal forms8,9, underpins the morphological hourglass pattern. Here we address this question using species-specific microarrays designed from six sequenced Drosophila species separated by up to 40 million years. We quantify divergence at different times during embryogenesis, and show that expression is maximally conserved during the arthropod phylotypic period. By fitting different evolutionary models to each gene, we show that at each time point more than 80% of genes fit best to models incorporating stabilizing selection, and that for genes whose evolutionarily optimal expression level is the same across all species, selective constraint is maximized during the phylotypic period. The genes that conform most to the hourglass pattern are involved in key developmental processes. These results indicate that natural selection acts to conserve patterns of gene expression during mid-embryogenesis, and provide a genome-wide insight into the molecular basis of the hourglass pattern of developmental evolution.

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Figure 1: Gene expression during Drosophila embryogenesis recapitulates the known phylogeny.
Figure 2: Temporal expression divergence is minimized during the phylotypic period.
Figure 3: Properties of genes with different divergence patterns.

Accession codes

Primary accessions

ArrayExpress

Data deposits

The expression data are available for download fromArrayExpress under experiment name ‘hourglass’, accession number E-MTAB-404, and together with the probe sequences at http://publications.mpi-cbg.de/4240-data.

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Acknowledgements

We thank A. Alexa for providing modified code for his topGO R package, A. Larracuente and T. Sackton for sharing data with us, M. Weber for generating the embryo images for Fig. 2, and Carl Zeiss MicroImaging for providing the SPIM microscope. We also thank N. Barton, T. Bedford, D. Hartl, J. Howard, A. Oates and D. Robertson for providing useful comments and discussion on the manuscript. This work was funded by The Human Frontier Science Program (HFSP) Young Investigator’s Grant RGY0084.

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K.M.V. and P.T. conceived the experiment, and K.M.V. and J.J. carried it out. K.M.V., P.T. and S.P. designed the microarray. P.T. conducted the interspecies correlation analysis, and S.P. formulated the linear interpolation algorithm. A.T.K. conceived and conducted the statistical analyses. D.T.G. and C.M.B. conducted the genomic correlates analysis. D.L.C. and U.O. carried out the probe orthology assignments. C.M.B. brought the hourglass concept to the attention of the HFSP team. A.T.K. wrote the paper with support from co-authors.

Corresponding author

Correspondence to Pavel Tomancak.

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The authors declare no competing financial interests.

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The file contains Supplementary Figures 1-11 with legends, Supplementary Tables 1-11, Supplementary Methods, Supplementary Results, a Supplementary Discussion and Supplementary References. (PDF 4042 kb)

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Kalinka, A., Varga, K., Gerrard, D. et al. Gene expression divergence recapitulates the developmental hourglass model. Nature 468, 811–814 (2010). https://doi.org/10.1038/nature09634

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