Current Biology 23(125): R510-R512 (2013)
Polygenic sex determination
Emily C. Moore and Reade B. Roberts

How is polygenic sex determination different? In the XY and ZW systems described above, a single genetic locus, often on a morphologically distinct chromosome, acts as the master switch for sex determination. In polygenic sex determination (PSD), multiple, independently segregating sex ‘switch’ loci or alleles determine sex within a species. Polygenic systems can arise through modifications of existing sex chromosomes that create a third functional sex chromosome at the same locus, or through modifications of autosomal loci elsewhere in the genome that create new inputs for regulation of gonad development. The term ‘polygenic sex determination’ appears to have been coined by Kosswig around 1964, shortly after PSD was described in platyfish (Xiphophorus spp.). In the case of platyfish, some populations have both a Y male determination allele and a W female determination allele segregating at the same chromosome pair. Despite the discovery and description of PSD nearly fifty years ago, the phenomenon remains relatively unknown, and only recently have we begun realizing the potential extent of PSD systems across taxa.

In PSD, which sex determination locus ‘wins’ to determine sex? The locus that wins and ultimately determines the fate of the gonad depends on the system being examined (Figure 1). In platyfish, pygmy mice, and lemmings, the ancestral state was an XY system. In these cases, one of the X chromosomes gained a female sex-determination allele that is dominant to the Y, directing ovary development in WY (also referred to as X*Y) individuals. Some species of cichlid fish from Lake Malawi have an XY locus and a WZ locus on distinct chromosome pairs, and when these occur in the same individual, the W female determiner wins, and the individual develops as female. The end result of PSD is not always skewed towards females; in some housefly populations, a sex determination locus on an autosome causes XX flies to develop as male. In other cases, including zebrafish and cichlids, sex determination likely results from a combination of additive and epistatic effects at many loci. Thus, an allele that wins in one combination of sex determination loci genotypes may lose in another. Indeed, in some gynodioecious plants, the outcome of a genetic contest between ‘anti-male’ mitochondrial loci and nuclear ‘pro-male’ restorer loci ultimately determines female versus hermaphrodite development. Truly, there is striking diversity in the different ways PSD has independently evolved across these taxa.

How many sexes are there? The traditional view of primary, gonadal sex is of a binary trait — each individual is either male or female. With multiple interacting loci determining primary sex, there are as many genetic sexes for a given group as there are possible combinations of sex determination loci. In known cases of PSD in animals, primary sex remains binary, but evidence suggests that genotypically different individuals of the same primary sex can have differential reproductive success, as mentioned above. Thus, even though primary sex may be binary in these cases, PSD may produce different classes within a single sex, or individuals of the same primary sex with strikingly different secondary sexual characteristics. In some plants, PSD systems may produce what could be considered more than two sexes. For example, in the domesticated cantaloupe, Cucumis melo, multiple loci interact to produce four sexes, with andromonoecious, monoecious, gynoecious, and hermaphrodite individuals in some cultivars (though it is not clear if such a system occurs naturally). In light of the variability in the genetic controls of sex determination and development, it may be beneficial to re-evaluate our view of sex as a binary trait.

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