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A battle between the sexes in a single gene


Enlarge / This female fruit fly wants Apollo out of her ovaries.

Evolution is great at driving changes when a species has specific needs. But what happens when different members of the same species need different things?

If those different groups are just different populations, that’s a recipe for a split into two new species. But in many cases, the issue comes about because males and females have different needs. That makes speciation a lousy solution (unless you can get rid of the males). What you end up with is a battle between the sexes that plays out in their genes, as changes that are good for females are balanced against the harm they do to males and vice versa. Now, researchers have identified one of these cases in fruit flies, and they figured out how the battle was resolved so that everyone mostly wins.

The Greek gods of fruit flies

In this case, the site of the battle is a small chunk of the genome that contains two genes: Apollo and Artemis. The genes aren’t just close to each other—they’re closely related as well. Approximately 200,000 years ago, a single ancestral gene was duplicated to produce these two. Closely related species of Drosophila only have a single copy of this gene.

Apollo clearly has an important function. If you eliminate the gene, survival goes down by about a third in both sexes, and all the surviving males are sterile. Flies seem to tolerate the loss of Artemis better, but when it’s eliminated, all the females end up sterile. All of which suggests that the ancestral gene played a critical role in both sexes’ fertility, and the duplication allowed each copy to be specialized for one sex.

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But the striking thing is that the specialization is actively harmful to the opposite sex. Males without a working copy of the Artemis gene—the one needed in females—actually produced 15 percent more offspring. And females with a mutation in Artemis produced about 20 percent more offspring. The conclusion from this is that when the gene is adapted to perform a function that males need, it actively interferes with female reproduction. The converse is also true.

Opposite sexes

In Drosophila melanogaster, the standard lab fruit fly, this problem is partly managed by the fact that Apollo shows much higher activity in the male germ cells than the female equivalents. Artemis, as you’d expect, is more active in female germ cells.

It’s not clear how related species handle the fact that they only have one copy of the gene and can’t have it specialized for just one sex. But a search through the genomes of other fruit fly species shows that it has been duplicated at least three other times. And the researchers found that, in each of these cases, the two copies had opposite expression levels in the two sexes.

So what’s going on with these genes? A look at the DNA sequence suggests they encode proteins that help control the structure of an internal mesh of fibers that act a bit like a cell’s skeleton. In males, the protein encoded by Apollo is needed for the cell division that is the final step in sperm production. In females that lack Artemis, the eggs that form are unusually large and can’t be fertilized. Plus there’s some essential function in both sexes (remember, a third of both males and females die when Apollo is knocked out), which hasn’t been identified yet.

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The two genes, despite being closely related, also have some key differences. There are now about a dozen individual changes in the amino acids used to make the protein, and the nearby DNA has picked up both an insertion (an intron) and several deletions. The critical difference (which hasn’t been identified yet) seems to have occurred about 50,000 years ago, when a copy of the genes was advantageous enough to quickly sweep through the entire fruit fly population.

While there are a lot of details of these genes that still need to be worked out, the overall evolutionary picture here is pretty clear. It’s also likely to be relevant to more than just fruit flies. Producing eggs and sperm are very different processes in mammals, too, and both processes are likely to require some specialized proteins. And duplications of genes are common enough that we can often detect a few when we compare a child’s genome to that of their parents.

Nature Ecology & Evolution, 2018. DOI: 10.1038/s41559-018-0471-0  (About DOIs).

A battle between the sexes in a single gene

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