Trends in Genetics
Volume 28, Issue 4, April 2012, Pages 175-184
Journal home page for Trends in Genetics

Review
Dmrt genes in the development and evolution of sexual dimorphism

https://doi.org/10.1016/j.tig.2012.02.002Get rights and content

Most animals are sexually dimorphic, but different taxa have different sex-specific traits. Despite major differences in the genetic control of sexual development among animal lineages, the doublesex/mab-3 related (Dmrt) family of transcription factors has been shown to be involved in sex-specific differentiation in all animals that have been studied. In recent years the functions of Dmrt genes have been characterized in many animal groups, opening the way to a broad comparative perspective. This review focuses on the similarities and differences in the functions of Dmrt genes across the animal kingdom. I highlight a number of common themes in the sexual development of different taxa, discuss how Dmrt genes have acquired new roles during animal evolution, and show how they have contributed to the origin of novel sex-specific traits.

Section snippets

Dmrt genes: a common theme amidst diversity

Sexual dimorphism (see Glossary) is one of the most pervasive and diverse features of animal morphology, physiology, and behavior. The demands of sexual reproduction and competition for mates have led each animal lineage to evolve its own suite of sex-specific characters. Lion manes, butterfly wings and bird songs seem to have nothing in common beyond the fact that they differ between males and females. The molecular mechanisms responsible for sexual dimorphism are almost as diverse, ranging

A deeply conserved role in gonad development

Although virtually every animal lineage has evolved its own somatic sex-specific characters, the one trait most animals have in common is the presence of sexually dimorphic gonads. Despite profound differences in gonad structure and development among animal phyla, Dmrt genes are specifically expressed in the developing gonads of almost all animals: in vertebrates including mammals 4, 12, 13, birds [7], turtles and alligators 14, 15, amphibians [9], and teleost fishes [8]; in arthropods

Somatic sexual dimorphism – integration of sex and pattern

The nature and development of sex-specific somatic traits show great diversity among animals, but once again the Dmrt genes emerge as one of the few common features. Their roles in sexual differentiation are best understood in Drosophila and C. elegans, where sex determination is largely cell-autonomous (Box 1). In flies, recent work has shown that dsx is transcribed in tightly controlled spatial patterns. Most cells of both male and female flies do not express either dsx isoform, resulting in

Non-autonomous control of sexual dimorphism

Precise spatial regulation of Dmrt genes is essential for normal development in animals as diverse as insects, vertebrates and nematodes. In all these systems, most cells do not express Dmrt genes. However, the relatively small populations of Dmrt-expressing cells can have a profound influence on sexual differentiation in the rest of the body. The most obvious of these roles is the endocrine control of vertebrate sexual differentiation. For example, the mammalian Sertoli cells, whose

Evolutionary takeovers of sex determination

Sex-determination signals and mechanisms evolve so rapidly that the master gene rarely stays at the top of the hierarchy for very long. For example, Sry does not exist outside mammals [52], whereas Sex-lethal (Sxl) (Box 1) exists but does not play a sex-determining role outside drosophilids 10, 11. In other lineages, sex-determining mechanisms turn over even more rapidly and can differ within species or between sibling species 53, 54. In vertebrates, the gonad controls sex-specific

Sex-specific splicing: an evolutionary switch in regulatory activity

A comparison of Dmrt genes from different animal lineages reveals important differences in their molecular functions despite their conserved roles in sexual differentiation. The mouse DMRT1 is a bifunctional regulator, activating some direct targets and repressing others [29]. The molecular basis of this versatility is unknown, but may involve the recruitment of different cofactors (coactivators vs corepressors) to the enhancers of different DMRT-regulated genes. The nematode MAB-3 is only

Origin and evolution of new sex-specific traits

One of the most fascinating features of animal evolution is the rapid turnover of sex-specific traits. Both lions and gazelles are sexually dimorphic, but the traits distinguishing males from females are clearly different between the two. This simple observation implies that new sexual characters are gained, and old ones are lost, during the evolution of any animal lineage. The molecular mechanisms of this turnover are poorly understood, but recent evidence suggests that Dmrt genes may play

Concluding remarks

Despite the endlessly diverse manifestations of sexual dimorphism and the profound differences between the mechanisms that specify it in different phyla, Dmrt genes provide a common framework for understanding the development and evolution of sex-specific traits. In all animals studied to date, members of the Dmrt family are expressed in tightly restricted spatial patterns in association with the development of sex-specific organs. Superficial differences between the roles of these genes in

Acknowledgments

I am grateful to David Loehlin for providing Nasonia images, and to David Plachetzki, Joël Savard, David Zarkower and three anonymous reviewers for their comments on the manuscript. Work in my laboratory is supported by National Institutes of Health grant 5-R01GM082843-02.

Glossary

Bilateria
a group of animal phyla that evolved from a common bilaterally symmetric ancestor; it includes all multicellular animals except the phyla Porifera, Placozoa, Cnidaria and Ctenophora.
Cell-autonomous gene function
developmental mechanism where the expression of a regulatory gene in a particular cell determines the fate or functional properties of that same cell.
Cis-regulatory changes
nucleotide substitutions in non-coding gene sequences that result in altered expression of that gene in the

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