In humans and other animals, sex is usually determined by a single gene. However, there are claims that in some species, such as platyfish, it takes an entire “parliament” of interacting genes to determine whether offspring develop as male or female.
In a new analysis, we took a closer look at these claims. We found that they describe abnormal situations, such as hybrids between two species with different sex-determining systems, or when one sex system is in the process of replacing the other.
We conclude that sex is normally determined by a single gene. The theory of evolution suggests that this is the most stable state of affairs, as it provides a 1:1 ratio of males to females.
The human ‘master switch’ for sex
In mammals, females have two X chromosomes, while males have an X and a Y. The Y chromosome carries a gene called SRY, which acts as a “master switch”: an XY embryo, carrying SRY, develops into a biological male, and an XX embryo, without SRY, develops into a biological female .
This makes the inheritance of sex simple. Females make eggs, which carry a single X chromosome, while males make sperm, half with an X and half with a Y.
Random fusion of eggs and sperm produces half XX females and half XY males, for a sex ratio of 1:1.
Sex in other vertebrates
Among animals with backbones (vertebrates), there is a huge variety of sex-determining systems. However, they usually boil down to the action of a single gene.
Have lots of fish, frogs and some turtles systems like ours, in which a male-dominant gene on the Y chromosome directs testicular development. Some vertebrates have the opposite: a female-dominant gene on the X chromosome.
Using other vertebrates a dose difference of a single gene. In birds, males have two copies of a Z chromosome containing the sex-determining gene DMRT1. Females have a single Z and a W chromosome without DMRT1. Gender depends on DMRT1 dose: two copies in ZZ males, versus one in ZW females.
Read more: How birds become male or female, and sometimes both
Surprisingly, many different genes act as the main switch in different types. But they all work by triggering the same male or female differentiation pathway.
These single-gene systems yield an equal number of males and females, which is theorized to be the optimal balance for a stable system. If the ratio is in favor of one sex, individuals producing more of the opposite sex will leave more offspring and their genes will spread until a ratio of 1:1 is reached.
Some exceptional species
Some aquarium fish to have more complex systems. Genetic crosses in platyfish appear to show two or more genes determining male or female development; the sea bass appears to have at least three sex genes.
Some frogs and lizards appear to determine sex using two or more sex genes.
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Then there are species with two or more pairs of sex chromosomes. The platypus has five X and five Y chromosomes. Is there a sex gene on each Y? How will a poor platypus know how to develop when it gets three Y’s and two X’s from its father?
And what about species, such as the African clawed toadwho have two copies of their entire genome, so should have two pairs of sex chromosomes and sex genes?
Thus, there are many exceptional species that seem to have multiple sex chromosomes and sex genes, despite the expectation that only one sex gene can produce a stable system.
Polygenic sex – does such a thing exist?
In species where we cannot find a single master switch gene, it is common to talk about “polygenic sex”. But how robust are these examples?
In our recent paper we examine classic examples and recent claims for polygenic sex determination. We conclude that the few systems that qualify for this represent anomalous and transient situations.
Multiple sex chromosomes need not mean multiple sex genes. At the platypus, all five Y chromosomes move together in sperm, and a single gene on the smallest Y directs male development. The African clawed toad dissolved the problem of his duplicated genome by developing a new female determinant gene on a newly minted W chromosome.
Two sex genes are detected in different systems, but they control different steps of the same pathway that are regulated by a single master gene.
In some classic fish systems, such as platyfish, the different variants all originate from the same chromosome, suggesting that sex is controlled by different variants of the same gene. A Japanese frog has different sex chromosomes on different islandsbut they are all variants of the same chromosome.
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Other examples suggest systems in transition. Sea bass shows different frequencies of variants across its range. There are signs that a new system is gradually replacing an old system a European frog.
The zebrafish is particularly interesting. Strains that have been independently grown in labs for 30 or 40 years have different sex ratios and multiple sex genes.
But it turns out that wild zebrafish have a regular ZW sex chromosome system. Lab strains independently lost their W chromosome during lab breeding. All lab fish are ZZ and the sex of the fry is determined by weaker sex-distinctive genes lurking in wait.
Winning the war of the sex genes
Many “polygenic” systems turn out to be hybrids between two species. Interspecies hybrids often have reproductive problems, such as infertility or skewed sex ratios.
Their problem is the incompatibility of different sex chromosomes and sex genes. When an XY male mates with a ZW female, offspring will have all kinds of combinations of sex genes.
Incompatibilities can turn out differently. For example, two types of cichlids that live side by side in Lake Malawi in Africa have unrelated XY and ZW systems. In their XYZW offspring, the W partially overrides the male-determining effect of the Y, so XYZW fish have intersex traits. But in another species combination, the W gene prevails and XYZW fish are fertile females.
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Species hybrids can reveal many genes with major and minor effects on sex determination. For example, crossing of two catfish speciess revealed seven male-associated and 17 female-associated genes on different chromosomes.
So there are certainly species in which two or more genes work together or against each other. In the long run, however, there is strong selection for one or the other to gain the upper hand. This will turn an inefficient polygenic system into a single gene system, producing fertile males and females in a 1:1 ratio.
Read more: Men are slowly losing their Y chromosome, but a new sex gene discovery in spiny rats brings hope to humanity
