Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development
Developmental conservation among related species is a common generalization known as von Baer's third law and implies that early stages of development are the most refractory to change. The "hourglass model" is an alternative view that proposes that middle stages are the most constrai...
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2013
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| Acceso en línea: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17596653_v5_n11_p2231_Mensch http://hdl.handle.net/20.500.12110/paper_17596653_v5_n11_p2231_Mensch |
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paper:paper_17596653_v5_n11_p2231_Mensch2023-06-08T16:29:01Z Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development Dosage compensation Embryonic genes Hourglass model Nups Drosophila protein nucleoporin animal article developmental gene Drosophila melanogaster embryonic genes gene gene expression regulation genetic selection genetics hourglass model molecular evolution Nups prenatal development dosage compensation embryonic genes hourglass model Nups Animals Dosage Compensation, Genetic Drosophila melanogaster Drosophila Proteins Evolution, Molecular Genes, Developmental Genes, Insect Nuclear Pore Complex Proteins Selection, Genetic Developmental conservation among related species is a common generalization known as von Baer's third law and implies that early stages of development are the most refractory to change. The "hourglass model" is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes, our results showed differential selective pressures at different moments of embryogenesis. In many Drosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. Because many Nups are involved in hybrid incompatibilities between species of the Drosophila melanogaster subgroup, our results link rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence. © The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2013 https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17596653_v5_n11_p2231_Mensch http://hdl.handle.net/20.500.12110/paper_17596653_v5_n11_p2231_Mensch |
| institution |
Universidad de Buenos Aires |
| institution_str |
I-28 |
| repository_str |
R-134 |
| collection |
Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) |
| topic |
Dosage compensation Embryonic genes Hourglass model Nups Drosophila protein nucleoporin animal article developmental gene Drosophila melanogaster embryonic genes gene gene expression regulation genetic selection genetics hourglass model molecular evolution Nups prenatal development dosage compensation embryonic genes hourglass model Nups Animals Dosage Compensation, Genetic Drosophila melanogaster Drosophila Proteins Evolution, Molecular Genes, Developmental Genes, Insect Nuclear Pore Complex Proteins Selection, Genetic |
| spellingShingle |
Dosage compensation Embryonic genes Hourglass model Nups Drosophila protein nucleoporin animal article developmental gene Drosophila melanogaster embryonic genes gene gene expression regulation genetic selection genetics hourglass model molecular evolution Nups prenatal development dosage compensation embryonic genes hourglass model Nups Animals Dosage Compensation, Genetic Drosophila melanogaster Drosophila Proteins Evolution, Molecular Genes, Developmental Genes, Insect Nuclear Pore Complex Proteins Selection, Genetic Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| topic_facet |
Dosage compensation Embryonic genes Hourglass model Nups Drosophila protein nucleoporin animal article developmental gene Drosophila melanogaster embryonic genes gene gene expression regulation genetic selection genetics hourglass model molecular evolution Nups prenatal development dosage compensation embryonic genes hourglass model Nups Animals Dosage Compensation, Genetic Drosophila melanogaster Drosophila Proteins Evolution, Molecular Genes, Developmental Genes, Insect Nuclear Pore Complex Proteins Selection, Genetic |
| description |
Developmental conservation among related species is a common generalization known as von Baer's third law and implies that early stages of development are the most refractory to change. The "hourglass model" is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes, our results showed differential selective pressures at different moments of embryogenesis. In many Drosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. Because many Nups are involved in hybrid incompatibilities between species of the Drosophila melanogaster subgroup, our results link rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence. © The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. |
| title |
Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| title_short |
Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| title_full |
Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| title_fullStr |
Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| title_full_unstemmed |
Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development |
| title_sort |
positive selection in nucleoporins challenges constraints on early expressed genes in drosophila development |
| publishDate |
2013 |
| url |
https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17596653_v5_n11_p2231_Mensch http://hdl.handle.net/20.500.12110/paper_17596653_v5_n11_p2231_Mensch |
| _version_ |
1768545948728819712 |