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Developmental constraints shape the evolution of the nematode mid-developmental transition

ABSTRACT: Evolutionary theory assumes that genetic variation is uniform and gradual in nature, yet morphological and gene expression studies have revealed that different life-stages exhibit distinct levels of cross-species conservation. In particular, a stage in mid-embryogenesis is highly conserved across species of the same phylum, suggesting that this stage is subject to developmental constraints, either by increased purifying selection or by a strong mutational bias. An alternative explanation, however, holds that the same ‘hourglass’ pattern of variation may result from increased positive selection at the earlier and later stages of development. To distinguish between these scenarios, we examined gene expression variation in a population of the nematode C. elegans using an experimental design that eliminated the influence of positive selection. By measuring gene expression for all genes throughout development in twenty strains, we found that variations were dramatically uneven throughout development, with a significant depletion during mid-embryogenesis. In particular, the family of homeodomain transcription factors, whose expression generally coincides with mid-embryogenesis, evolved under high constraint. Our data further shows that genes responsible for the integration of germ layers during morphogenesis are the most constrained class of genes. Together, these results provide the first evidence for developmental constraints as the mechanism underlying the hourglass model of animal evolution. Understanding the pattern and mechanism of developmental constraints provides a framework to understand how evolutionary processes have interacted with embryogenesis and led to the diversity of animal life on earth.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE87528 | GEO | 2017/04/04

SECONDARY ACCESSION(S): PRJNA345017

REPOSITORIES: GEO

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Project description:The M-bM-^@M-^Xdevelopmental hourglassM-bM-^@M-^Y concept suggests that intermediate developmental stages are most resistant to evolutionary changes and that differences between species arise through divergence later in development. This high conservation during mid-development is illustrated by the M-bM-^@M-^XwaistM-bM-^@M-^Y of the hourglass and it represents a low probability of evolutionary change. Earlier molecular surveys both on animals and plants have shown that the genes expressed at the waist stage are more ancient and more conserved in their expression. The existence of such a developmental hourglass has not been explored in fungi, another eukaryotic kingdom. In this study, we generated a series of transcriptomic data covering the entire lifecycle of a model mushroom-forming fungus, Coprinopsis cinerea, and we observed a molecular hourglass over its development. The M-bM-^@M-^Xyoung fruiting bodyM-bM-^@M-^Y (YFB) is the stage that expresses the evolutionarily oldest (lowest transcriptome age index, TAI) transcriptome and gives the strongest signal of purifying selection (lowest transcriptome divergence index, TDI). We also demonstrated that all three kingdoms M-bM-^@M-^S animals, plants and fungi M-bM-^@M-^S display high expression levels of genes in M-bM-^@M-^Xinformation storage and processingM-bM-^@M-^Y at the waist stages, whereas the genes in M-bM-^@M-^XmetabolismM-bM-^@M-^Y become more highly expressed later. Besides, the three kingdoms all show underrepresented M-bM-^@M-^Xsignal transductionM-bM-^@M-^Y at the waist stages. The synchronic existence of a molecular M-bM-^@M-^XhourglassM-bM-^@M-^Y across the three kingdoms reveals a mutual strategy for eukaryotes to incorporate evolutionary innovations. NimbleGen custom microarray with total RNAs extracted from two biological replicates for each stage of mycelium, fruiting initials (~2mm tall), stage 2 primordium (~1cm tall), young fruiting body (~2cm tall) and the fully-expanded cap of the mature fruiting body (~4cm tall). Mycelia from 5 agar plates were collected and pooled to form one replicate. For the other stages, 4-5 independent structures were isolated and their RNA extracted as one replicate sample.

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Developmental constraints shape the evolution of the nematode mid-developmental transition

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