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The hourglass and the early conservation models--co-existing patterns of developmental constraints in vertebrates.

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.

SUBMITTER: Piasecka B

PROVIDER: S-EPMC3636041 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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The hourglass and the early conservation models--co-existing patterns of developmental constraints in vertebrates.

Piasecka Barbara B Lichocki Paweł P Moretti Sébastien S Bergmann Sven S Robinson-Rechavi Marc M

PLoS genetics 20130425 4

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 ...[more]

PMID: 23637639

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Project description:BackgroundThe Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model.ResultsThe genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family.ConclusionDlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.

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.

Dataset Information

The hourglass and the early conservation models--co-existing patterns of developmental constraints in vertebrates.

Publications

The hourglass and the early conservation models--co-existing patterns of developmental constraints in vertebrates.

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