An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.

The X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosome...

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Main Authors: Melek A Kayserili, Dave T Gerrard, Pavel Tomancak, Alex T Kalinka
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003200&type=printable
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author Melek A Kayserili
Dave T Gerrard
Pavel Tomancak
Alex T Kalinka
author_facet Melek A Kayserili
Dave T Gerrard
Pavel Tomancak
Alex T Kalinka
author_sort Melek A Kayserili
collection DOAJ
description The X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosomes, suggesting that the X might be more strongly affected by genetic drift. However, the X may also experience stronger positive selection than the autosomes, because recessive beneficial mutations will be more visible to selection on the X where they will spend less time being masked by the dominant, less beneficial allele--a proposal known as the faster-X hypothesis. Thus, empirical studies demonstrating increased genetic divergence on the X chromosome could be indicative of either adaptive or non-adaptive evolution. We measured gene expression in Drosophila species and in D. melanogaster inbred strains for both embryos and adults. In the embryos we found that expression divergence is on average more than 20% higher for genes on the X chromosome relative to the autosomes; but in contrast, in the inbred strains, gene expression variation is significantly lower on the X chromosome. Furthermore, expression divergence of genes on Muller's D element is significantly greater along the branch leading to the obscura sub-group, in which this element segregates as a neo-X chromosome. In the adults, divergence is greatest on the X chromosome for males, but not for females, yet in both sexes inbred strains harbour the lowest level of gene expression variation on the X chromosome. We consider different explanations for our results and conclude that they are most consistent within the framework of the faster-X hypothesis.
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spelling doaj-art-f8f8d8c038c74c7b84e6935d9a94c28c2025-08-20T03:01:15ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-01812e100320010.1371/journal.pgen.1003200An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.Melek A KayseriliDave T GerrardPavel TomancakAlex T KalinkaThe X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosomes, suggesting that the X might be more strongly affected by genetic drift. However, the X may also experience stronger positive selection than the autosomes, because recessive beneficial mutations will be more visible to selection on the X where they will spend less time being masked by the dominant, less beneficial allele--a proposal known as the faster-X hypothesis. Thus, empirical studies demonstrating increased genetic divergence on the X chromosome could be indicative of either adaptive or non-adaptive evolution. We measured gene expression in Drosophila species and in D. melanogaster inbred strains for both embryos and adults. In the embryos we found that expression divergence is on average more than 20% higher for genes on the X chromosome relative to the autosomes; but in contrast, in the inbred strains, gene expression variation is significantly lower on the X chromosome. Furthermore, expression divergence of genes on Muller's D element is significantly greater along the branch leading to the obscura sub-group, in which this element segregates as a neo-X chromosome. In the adults, divergence is greatest on the X chromosome for males, but not for females, yet in both sexes inbred strains harbour the lowest level of gene expression variation on the X chromosome. We consider different explanations for our results and conclude that they are most consistent within the framework of the faster-X hypothesis.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003200&type=printable
spellingShingle Melek A Kayserili
Dave T Gerrard
Pavel Tomancak
Alex T Kalinka
An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
PLoS Genetics
title An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
title_full An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
title_fullStr An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
title_full_unstemmed An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
title_short An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis.
title_sort excess of gene expression divergence on the x chromosome in drosophila embryos implications for the faster x hypothesis
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003200&type=printable
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