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Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull.

ABSTRACT: Development of the vertebrate skull has been studied intensively for more than 150 years, yet many essential features remain unresolved. One such feature is the extent to which embryonic derivation of individual bones is evolutionarily conserved or labile. We perform long-term fate mapping using GFP-transgenic axolotl and Xenopus laevis to document the contribution of individual cranial neural crest streams to the osteocranium in these amphibians. Here we show that the axolotl pattern is strikingly similar to that in amniotes; it likely represents the ancestral condition for tetrapods. Unexpectedly, the pattern in Xenopus is much different; it may constitute a unique condition that evolved after anurans diverged from other amphibians. Such changes reveal an unappreciated relation between life history evolution and cranial development and exemplify 'developmental system drift', in which interspecific divergence in developmental processes that underlie homologous characters occurs with little or no concomitant change in the adult phenotype.

SUBMITTER: Piekarski N

PROVIDER: S-EPMC4251486 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull.

Piekarski Nadine N Gross Joshua B JB Hanken James J

Nature communications 20141201

Development of the vertebrate skull has been studied intensively for more than 150 years, yet many essential features remain unresolved. One such feature is the extent to which embryonic derivation of individual bones is evolutionarily conserved or labile. We perform long-term fate mapping using GFP-transgenic axolotl and Xenopus laevis to document the contribution of individual cranial neural crest streams to the osteocranium in these amphibians. Here we show that the axolotl pattern is strikin ...[more]

PMID: 25434971

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Project description:BackgroundUnderstanding the general trends in developmental changes during animal evolution, which are often associated with morphological diversification, has long been a central issue in evolutionary developmental biology. Recent comparative transcriptomic studies revealed that gene expression profiles of mid-embryonic period tend to be more evolutionarily conserved than those in earlier or later periods. While the hourglass-like divergence of developmental processes has been demonstrated in a variety of animal groups such as vertebrates, arthropods, and nematodes, the exact mechanism leading to this mid-embryonic conservation remains to be clarified. One possibility is that the mid-embryonic period (pharyngula period in vertebrates) is highly prone to embryonic lethality, and the resulting negative selections lead to evolutionary conservation of this phase. Here, we tested this "mid-embryonic lethality hypothesis" by measuring the rate of lethal phenotypes of three different species of vertebrate embryos subjected to two kinds of perturbations: transient perturbations and genetic mutations.ResultsBy subjecting zebrafish (Danio rerio), African clawed frog (Xenopus laevis), and chicken (Gallus gallus) embryos to transient perturbations, namely heat shock and inhibitor treatments during three developmental periods [early (represented by blastula and gastrula), pharyngula, and late], we found that the early stages showed the highest rate of lethal phenotypes in all three species. This result was corroborated by perturbation with genetic mutations. By tracking the survival rate of wild-type embryos and embryos with genetic mutations induced by UV irradiation in zebrafish and African clawed frogs, we found that the highest decrease in survival rate was at the early stages particularly around gastrulation in both these species.ConclusionIn opposition to the "mid-embryonic lethality hypothesis," our results consistently showed that the stage with the highest lethality was not around the conserved pharyngula period, but rather around the early period in all the vertebrate species tested. These results suggest that negative selection by embryonic lethality could not explain hourglass-like conservation of animal embryos. This highlights the potential contribution of alternative mechanisms such as the diversifying effect of positive selections against earlier and later stages, and developmental constraints which lead to conservation of mid-embryonic stages.

Dataset Information

Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull.

Publications

Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull.

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