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Sex-chromosome evolution: recent progress and the influence of male and female heterogamety

A Corrigendum to this article was published on 16 September 2011

This article has been updated

Key Points

  • Sex chromosomes are unusually labile systems, with frequent shifts between male and female heterogamety and with a large variety in the precise number and types of chromosomes.

  • The lability is further emphasized by rapid turnover of genes and gene organization on the Y chromosome.

  • All types of sex chromosome (X, Y, Z and W) contain ampliconic structures of multi-copy genes.

  • A common model of sex-chromosome evolution implies gradual cessation of recombination between the proto-sex chromosomes.

  • The gene content of the X chromosome and the Z chromosome is unusual, with a non-random representation of genes with sex-biased gene expression.

  • The molecular evolution of sex-linked genes differs from autosomal genes with respect to mutation rate and selective pressure.

Abstract

It is now clear that sex chromosomes differ from autosomes in many aspects of genome biology, such as organization, gene content and gene expression. Moreover, sex linkage has numerous evolutionary genetic implications. Here, I provide a coherent overview of sex-chromosome evolution and function based on recent data. Heteromorphic sex chromosomes are almost as widespread across the animal and plant kingdoms as sexual reproduction itself and an accumulating body of genetic data reveals interesting similarities, as well as dissimilarities, between organisms with XY or ZW sex-determination systems. Therefore, I discuss how patterns and processes associated with sex linkage in male- and female-heterogametic systems offer a useful contrast in the study of sex-chromosome evolution.

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Figure 1: Organization of the human X chromosome.
Figure 2: Organization of human and chimpanzee Y chromosomes.
Figure 3: Organization of the chicken Z chromosome.

Change history

  • 16 September 2011

    In figure 1a of the above article, the evolutionary strata (S1–S5) on the human X chromosome were incorrectly labelled. The figure showed the strata in the order S1 to S5, with S1 adjacent to the pseudoautosomal region. The order should be reversed (S5 to S1), with S5 adjacent to the pseudoautosomal region instead. The figure has been amended accordingly. The author apologizes for this error.

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Acknowledgements

Work in my laboratory is supported by the Swedish Research Council, a European Research Council Advanced Investigator Grant and a Knut and Alice Wallenberg Foundation Wallenberg Scholar Award. I thank S. Adolfsson and H. Johannesson for useful comments on the manuscript.

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Glossary

Sexual antagonism

Sexually antagonistic genes are genes for which expression has contrasting effects on fitness in the two sexes.

Gametologous

Gametologous genes are homologous genes shared between the X and Y, or Z and W, chromosomes that have evolved independently since recombination ceased in the ancestral gene.

Pseudoautosomal region

(PAR). The region of both sex chromosomes that still recombines in the heterogametic sex. In old and highly differentiated sex chromosomes, such as the mammalian X and Y, the PAR is usually small.

Gene conversion

The transfer of genetic material from one chromosomal region to another. The 'donor' locus remains intact whereas the 'acceptor' locus changes. Gene conversion occurs between more or less homologous sequences.

Granulosa cells

Somatic cells in the ovary that surround the oocyte.

Haldane's rule

The tendency for offspring of the heterogametic sex to suffer more severe fitness consequences from an interspecific mating (hybridization) than the homogametic sex.

Effective population size

(Ne). Indicates how many individuals actually contribute alleles to the next generation, as opposed to the actual number of individuals in a population. For various reasons, including the preferential reproduction of some individuals and population size fluctuations over time, the effective population size is typically smaller than the actual number of individuals in the population.

Muller's ratchet

A population of non-recombining chromosomes may — by chance or by selection for beneficial variants contained within other haplotypes — irreversibly lose the class of chromosomes that is least loaded with deleterious mutations. Like a ratchet, this is a unidirectional process that inevitably leads to the degeneration of non-recombining chromosomes.

Hill–Robertson interference

The general concept of selection at one locus affecting the efficiency of selection at a linked locus.

Selective sweep

A positive selection for an advantageous allele will increase the frequency of not only that allele but also other alleles contained within the same haplotype, causing a selective sweep (also referred to as genetic hitch-hiking). A hallmark of such sweeps is reduced levels of genetic diversity around the selected locus.

Background selection

Purifying (negative) selection against a deleterious allele will also tend to remove linked variants, or at least decrease their frequency, contributing to loss of genetic diversity (compare with selective sweep).

Chromosome painting

The use of an isolated chromosome, labelled with a fluorophore, as a probe in hybridization to a chromosome spread of the same or of a different species. The chromosomal regions homologous to the probe will be 'painted' and light up when fluorescence is detected.

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Ellegren, H. Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12, 157–166 (2011). https://doi.org/10.1038/nrg2948

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