Key Points
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Differences in mammalian oogenesis and spermatogenesis lead to a lower mutation rate on the X chromosome than on the autosomes.
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If new mutations are on average partially recessive, adaptive evolution will be more widespread on the X chromosome, whereas deleterious mutations will accumulate faster on the autosomes.
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Divergence and polymorphism data in Drosophila melanogaster and mammals suggest that, indeed, selection is more efficient on the X chromosome.
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Sexual-antagonism models predict that the X chromosome is a hot spot for sex-biased genes, as it will accumulate both dominant female-beneficial mutations and recessive male-beneficial mutations.
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Microarray data have shown a non-random distribution of sex-biased genes on the X chromosome and the autosomes, but the patterns differ between Caenorhabditis elegans, D. melanogaster and mammals.
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There is an excess of gene retroposition from the X chromosome to the autosomes in mammals and D. melanogaster.
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These new genes might be preserved by selection, as they are expressed in late spermatogenesis, when the X chromosome is inactivated.
Abstract
Although the X chromosome is usually similar to the autosomes in size and cytogenetic appearance, theoretical models predict that its hemizygosity in males may cause unusual patterns of evolution. The sequencing of several genomes has indeed revealed differences between the X chromosome and the autosomes in the rates of gene divergence, patterns of gene expression and rates of gene movement between chromosomes. A better understanding of these patterns should provide valuable information on the evolution of genes located on the X chromosome. It could also suggest solutions to more general problems in molecular evolution, such as detecting selection and estimating mutational effects on fitness.
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Acknowledgements
We thank H. Ellegren and V. Kaiser for providing us with their unpublished manuscript. B.V. is supported by a postgraduate fellowship from the Fundação de Ciência e Tecnologia of Portugal, and B.C. by the Royal Society (UK). We thank two anonymous reviewers for their comments, which helped to improve the manuscript.
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Glossary
- Haldane's rule
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The disproportionate loss of fitness to the heterogametic sex in F1 hybrids between species.
- Clade
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A group of species which share a common ancestor.
- Male heterogamety
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Describes the situation in which males carry two heteromorphic sex chromosomes (such as X and Y) and females carry two copies of the same chromosome (XX).
- Neutral DNA
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DNA that is not subject to selection.
- Silent nucleotide sites
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Nucleotides where mutations do not change protein sequences.
- CpG sites
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Adjacent cytosine and guanine bases in a DNA sequence.
- Fitness
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The expected contribution of an individual to the next generation.
- Genetic drift
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Random fluctuation of allele frequencies in a population due to sampling effects (as only a subsample of the gametic pool is used in each generation).
- Non-synonymous mutations
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Mutations that change the protein sequence; these are likely to be under selection.
- Fixation
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Increase of an allele frequency to 1.
- Positive selection
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Spread of a mutation through a population, because of increased survival or reproduction of the individuals carrying it.
- Purifying selection
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Removal of mutations from the population, because of reduced survival or reproduction of the individuals carrying it.
- Pseudogene
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A gene that has accumulated mutations in its protein-coding sequence or regulatory region, so that it is no longer functional.
- Codon bias
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Preferred usage of some codons over others that code for the same amino acid, possibly as a result of selection for increased translation efficiency or accuracy.
- Polymorphism
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Genetic variation within a species or population.
- Linkage disequilibrium
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Non-independent associations of alleles at different loci in a population.
- Ectopic recombination
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Recombination between homologous sequences that are located in different genomic locations. It can result in deletions and other types of chromosomal rearrangement.
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Vicoso, B., Charlesworth, B. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7, 645–653 (2006). https://doi.org/10.1038/nrg1914
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DOI: https://doi.org/10.1038/nrg1914
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