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Genetic and molecular insights into the development and evolution of sexual dimorphism

Nature Reviews Genetics volume 10, pages 797–804 (2009)Cite this article

A Corrigendum to this article was published on 01 December 2009

Key Points

  • Sexual dimorphism, or the morphological and behavioural differentiation of the two sexes of the same species, is widespread in nature.

  • Sex-limited traits are the product of sex-limited gene expression.

  • Although the mechanisms that initiate sexually dimorphic development are remarkably diverse, these pathways generally converge upon more conserved genetic components.

  • Gene cis-regulatory elements that possess binding sites for both sex- and tissue-specific transcription factors function as sexually dimorphic genetic switches in pathways for sexually dimorphic traits.

  • Effectors of the sexual differentiation pathway that are expressed specifically in the neural region can collaborate with other factors to generate sexually dimorphic neural morphology and hence behaviour.

  • New patterns of sex-limited gene expression and traits can evolve by the modification of ancestral cis-regulatory elements that control other dimorphic traits.

  • The gain and loss of binding sites for the transcriptional effectors of sexual differentiation pathways in cis-regulatory elements can result in the transition between sexually dimorphic and monomorphic gene expression.

  • The evolution of sexually dimorphic cis-regulatory elements in genes explains how the development of the two sexes can become uncoupled and allow for the independent evolution of traits between the sexes.

  • Evolutionary-developmental biologists have shown how sexually dimorphic traits arise, and ecologists have shown the importance of such traits in nature. An important future goal is to bridge the findings of these two disciplines.

Abstract

Sexual dimorphism is common throughout the animal kingdom. However, a molecular understanding of how sex-specific traits develop and evolve has been elusive. Recently, substantial progress has been made in elucidating how diverse sex-determination systems are integrated into developmental gene networks. One common theme from these studies is that sex-limited traits and gene expression are produced by the combined action of transcriptional effectors of sex-determination pathways and other transcription factors on target gene cis-regulatory elements. Sex-specific traits evolve by the gain, loss or modification of linkages in the genetic networks regulated by sex-determination transcription factors.

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Figure 1: Animal sexual dimorphism.
Figure 2: Sex-determination hierarchies.
Figure 3: Regulatory logic of sexually dimorphic genetic switches.
Figure 4: Two routes by which sexually dimorphic gene expression evolves.

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Acknowledgements

We thank three anonymous referees for their thoughtful critiques and suggestions to improve this manuscript. We are grateful to the following individuals for granting permission to use the images in figure 1: A. Wild, K. Lu, T. Bartlett, M. K. Meyer and C. Lambert. S.B.C. acknowledges research support from the Howard Hughes Medical Institute.

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Authors and Affiliations

  1. Department of Biology, University of Dayton, 300 College Park, Dayton, 45469, Ohio, USA

    Thomas M. Williams

  2. Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, 1525 Linden Drive, Madison, 53706, Wisconsin, USA

    Sean B. Carroll

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Correspondence to Sean B. Carroll.

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DATABASES

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dsx

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mab-3

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FURTHER INFORMATION

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Glossary

Sexually dimorphic traits

Any difference between males and females/hermaphrodites in appearance, cellular chemistry or behaviour.

Sex-limited gene expression

Any differences in the overall expression profile of a gene between males and females/hermaphrodites.

Cis-regulatory element

A discrete region of DNA adjacent to a gene that affects the expression level of the gene.

Heteromorphic sex chromosomes

Chromosomes that differ in appearance and gene content, are unequally shared between the sexes and function in sex determination.

Genetic balance

A mechanism of sex determination in which the quantity or dose of a particular sex chromosome rather than the content determines the sex of a zygote.

Hedgehog signalling

The hedgehog proteins are a class of secreted cell–cell signalling molecule. The name derives from the appearance of embryonic Drosophila melanogaster mutants that lack hedgehog gene function. There are many vertebrate genes that encode hedgehog homologues.

Bipotential gonad

The last embryonic tissue precursor that can differentiate into either the ovary or the testis.

Monotremes

Non-eutherian, egg-laying mammals.

Sertoli cell

A cell in the testis that secretes factors, including Müllerian inhibiting substance, and provides nourishment to early sperm cells.

Oviparous

Animals that reproduce by laying eggs that develop and hatch outside the mother's body.

Wattle

A fleshy coloured fold of skin hanging from the neck or throat of certain bird species.

Oenocytes

Specialized cells that lie underneath the dorsal and ventral cuticle of adult fruitfly abdomens. They are arranged in metameric transverse stripes that do not cross the midline of the body.

Mesothoracic ganglion

Part of the central nervous system that supplies motor neurons to the wing muscles of the mesothoracic segment.

Homeobox gene

A member of the family of genes that are largely involved in patterning the primary animal body axis during development. In many species, homeobox genes are clustered together on defined chromosomes and are often sequentially expressed.

Fitness

A quantity that is proportional to the mean number of viable, fertile progeny produced by a genotype.

Pleiotropic

The phenomenon by which a single gene is responsible for several distinct and seemingly unrelated phenotypic effects.

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Williams, T., Carroll, S. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat Rev Genet 10, 797–804 (2009). https://doi.org/10.1038/nrg2687

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