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Review
. 2010 Sep;186(1):9-31.
doi: 10.1534/genetics.110.117697.

The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals

Deborah Charlesworth  1 , Judith E Mank
Affiliations
Review

The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals

Deborah Charlesworth et al. Genetics. 2010 Sep.

Abstract

The ability to identify genetic markers in nonmodel systems has allowed geneticists to construct linkage maps for a diversity of species, and the sex-determining locus is often among the first to be mapped. Sex determination is an important area of study in developmental and evolutionary biology, as well as ecology. Its importance for organisms might suggest that sex determination is highly conserved. However, genetic studies have shown that sex determination mechanisms, and the genes involved, are surprisingly labile. We review studies using genetic mapping and phylogenetic inferences, which can help reveal evolutionary pattern within this lability and potentially identify the changes that have occurred among different sex determination systems. We define some of the terminology, particularly where confusion arises in writing about such a diverse range of organisms, and highlight some major differences between plants and animals, and some important similarities. We stress the importance of studying taxa suitable for testing hypotheses, and the need for phylogenetic studies directed to taxa where the patterns of changes can be most reliably inferred, if the ultimate goal of testing hypotheses regarding the selective forces that have led to changes in such an essential trait is to become feasible.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
Potential changes during the evolution of sex-determining regions from different possible starting states and possible changes in their subsequent evolution. In the evolution of dioecy from hermaphroditism, females are assumed to evolve first through a recessive male-sterility mutation. Starting from ESD, females might arise by loss of the ability to respond to an environmental trigger for male development. Males in either pathway then arise by a linked mutation causing failure to develop female structures, resulting in proto-sex chromosomes. Before recombination suppresssion has become extensive and genetic degeneration of one sex chromosome has occurred, the linkage group associated with sex determination can change by the replacement of a new sex-determining gene or via the transpositation of the existing sex-determining region to a new autosome. Translocations between the sex chromosomes and autosomes may also occur, and may involve either proto-sex chromosomes or degenerated ones.
F<sc>igure</sc> 2.—
Figure 2.—
Evolutionary strata are regions where recombination ceased at different times during sex chromosome evolution, as recombination suppression (open bars) spreads gradually over the length of the sex chromosomes. Regions where recombination ceased first have greater sequence divergence between X–Y or Z–W orthologous pairs of genes than regions where recombination ceased recently. In this illustration of an X–Y pair, sex-determining genes evolved in the initially recombining region labeled 1, and recombination ceased first in this region, creating stratum 1. This led to genetic degeneration of this stratum in the Y chromosome, and the evolution of chromosome heteromorphism. The process was repeated when recombination ceased in stratum 2, then stratum 3. The cessation of recombination in stratum 4 leaves only a small “pseudoautosomal region” on the X and Y chromosomes where recombination still occurs.
F<sc>igure</sc> 3.—
Figure 3.—
Sex determination in the actinopterygiian fishes (adapted from Mank et al. 2005, 2006). Shown is the supertree topology for the clade, presenting only the orders where sex determination is known for at least some members. Divergence dates of teleost clades are still contested and are therefore not indicated in the figure; however, it is helpful to note several nodes dated with a recently estimated molecular clock (Setiamarga et al. 2009). These include the origins of the Tetraodontiformes (80 MYA), the Beloniformes (115 MYA), the Salmoniformes (135 MYA), the Cypriniformes (190 MYA), and the Anguilliformes (220 MYA) and the divergence of the Gasterosteiformes from the Scorpaeniformes (150 MYA). Under environmental sex determination (ESD), we include sequential hermaphrodites where size plays a role in determining sex, as well as gonochorist species, where the environment can influence sex determination during development, and taxa with sequential hermaphrodites are noted separately (sim. herm.). Male heterogametic species are denoted by XY, even when there is no known chromosome heteromorphism, and female heterogametic species are similarly denoted by ZW. Sex determination in silversides has been shown to have a genetic component, although it is not known whether males or females are the heterozygous sex (Conover and Kynard 1981).
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