Ladies First: Genes skew sex ratios in evolutionary struggle

Competition among genes within an individual male fruit fly can cause its sperm to produce a high proportion of female offspring. Now, scientists have identified a gene responsible for this well-known phenomenon as well as the gene that later evolved to restore gender balance.

In essence, the two fruit fly genes engage in a tug-of-war in which each succeeds evolutionarily if it can spread widely among future generations.

The imbalance favoring females happens because the sex-skewing gene, called Distorter on the X (Dox), is located on the X chromosome. Females each have two X chromosomes, and pass on only Xs to their offspring. Males each have an X and a Y. They pass an X chromosome to their female offspring and a Y to their male offspring.

To ensure its evolutionary success, Dox somehow sabotages the maturation of sperm carrying Y chromosomes. As a result, a male fruit fly carrying Dox would produce a generation of offspring that is more than 90 percent Dox-carrying females.

This imbalance allows Dox to spread widely among a population in only a few generations, but the gene’s success sets the stage for its own defeat.

Once the population is dominated by females, a male will have many chances to reproduce and pass on its genes. This fact changes the game, because it means that a gene can now spread rapidly if it’s carried by a male.

The preponderance of females “creates a strong pressure for the evolution of a [Dox] suppressor gene,” says Yun Tao of Emory University in Atlanta, who led the research. If a gene on one of the nonsex chromosomes could shut down Dox, its odds of being passed on to male offspring would increase. Since the population is mostly female, males that inherit the suppressor gene would have many opportunities to breed and pass on the gene.

Indeed, Tao’s team found a gene that suppresses Dox. They dubbed it Not much yang (Nmy). Tao says that Nmy could have arisen in fruit flies only a few dozen generations after Dox first appeared. The researchers found that the two genes share regions of identical genetic code, which suggests that Nmy is simply an altered copy of Dox. That finding could explain how Nmy could have evolved so quickly, the researchers report in the November PLoS Biology.

The fact that the genes share genetic code could also explain how Nmy silences Dox. Molecular transcripts of Nmy would match up with and bind to transcripts of Dox, which would block the Dox transcripts from crippling a male’s Y-bearing sperm.

“It’s absolutely remarkable,” comments John Jaenike of the University of Rochester in New York, who has performed related research on skewed sex ratios. “This is the first report ever that identifies the suppressor and proposes an extremely elegant model of suppression.”

Fruit flies have at least two other pairs of sex-skewing and suppressing genes, but no one has managed to identify them. Tao says that it’s uncertain whether people carry similar gene pairs.