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The evolution of sex-biased genes and sex-biased gene expression

Nature Reviews Genetics volume 8, pages 689–698 (2007)Cite this article

Key Points

  • Sexual dimorphism in gene expression is widespread across organisms and genomes.

  • Genes with sex-biased expression, especially those with male-biased expression, tend to evolve rapidly in both protein sequence and expression level.

  • Sex-biased genes are non-randomly distributed in the genome, with examples of both under-representation and over-representation on the X chromosome.

  • There is mounting evidence that positive selection is the driving force behind the rapid evolution of sex-biased genes. This is probably caused by sexual selection and antagonistic coevolution between the sexes.

  • Sex-linked genes that escape dosage compensation constitute a special case of sex-biased gene expression.

  • There are several scenarios for the origin of sex-biased genes, including single-locus antagonism, sexual antagonism plus gene duplication and duplication of sex-biased genes.

Abstract

Differences between males and females in the optimal phenotype that is favoured by selection can be resolved by the evolution of differential gene expression in the two sexes. Microarray experiments have shown that such sex-biased gene expression is widespread across organisms and genomes. Sex-biased genes show unusually rapid sequence evolution, are often labile in their pattern of expression, and are non-randomly distributed in the genome. Here we discuss the characteristics and expression of sex-biased genes, and the selective forces that shape this previously unappreciated source of phenotypic diversity. Sex-biased gene expression has implications beyond just evolutionary biology, including for medical genetics.

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Figure 1: Fitness trade-offs for a sexually antagonistic mutation.
Figure 2: Divergence of sex-biased genes between Drosophila species.
Figure 3: Adaptive evolution of sex-biased genes.
Figure 4: Scenarios for the accumulation and underrepresentation of sexually antagonistic mutations on sex chromosomes.

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Acknowledgements

Financial support was obtained from the Swedish Research Council to H. E. and Deutsche Forschungsgemeinschaft to J. P.

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  1. Department of Evolutionary Biology, Uppsala University, Norbyvägen 18D, Uppsala, SE-752 36, Sweden

    Hans Ellegren

  2. Department of Biology II, Section of Evolutionary Biology, University of Munich (LMU), Munich, 82152, Germany

    John Parsch

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Glossary

Sexual dimorphism

Phenotypic differences between males and females of the same species.

Sexual selection

The process of natural selection acting on traits related directly to mating or reproductive success.

Sexual antagonism

Conflict arising from traits that are beneficial to one sex but harmful to the other.

Sex-biased genes

A gene that is expressed predominantly or exclusively in one sex.

Codon bias

The non-random use of synonymous codons to encode a protein.

dN/dS

The ratio of the non-synonymous (amino-acid altering) and synonymous substitution rates, used as a standard measure of the rate of evolution of a protein-encoding sequence.

EST sequencing

Large-scale sequencing of clones from a cDNA library obtained from mRNA.

Transcriptome profiling

A characterization of the mRNA molecules that are expressed in a certain tissue.

Androdioecious

A population consisting of hermaphrodites, which contain both male and female reproductive tissues, and males, which contain only male reproductive tissues.

Positive selection

Positive selection is key to adaptive evolution and implies that an advantageous allele gives its carrier a higher fitness and is therefore favoured by natural selection.

Fixation

When a new mutation is eventually spread to all individuals in the population.

Accessory glands

In insects, such as Drosophila, these are male reproductive tissues that produce and secrete seminal fluid proteins that are transferred to the female during copulation.

Purifying selection

Negative selection against a deleterious or slightly deleterious mutation.

Heterogametic sex

The sex that produces two different types of gametes with respect to sex chromosome content (for example, XY).

Homogametic sex

The sex that produces one type of gamete with respect to sex chromosome content (for example, XX).

Retrogene

A gene duplicate that arose through reverse transcription of a cellular mRNA.

Subfunctionalization

The partitioning of multiple ancestral gene functions between gene copies following duplication.

Neofunctionalization

A gain of a new function to a duplicated gene through mutation and selection.

Paralogues

Genes that arose from duplication of a common, ancestral gene. A gene that was duplicated before the divergence of two species is present as two paralogues, each of which has an orthologue in the other species.

Pleiotropy

The influence that a single gene has on multiple traits.

Epistatic selection

Selection for a certain combination of alleles at two or more loci.

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Ellegren, H., Parsch, J. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8, 689–698 (2007). https://doi.org/10.1038/nrg2167

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