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A ‘supergene’ turns these male birds into female impersonators or sneaky mate thieves — for life

The "satellite" ruff is a predetermined parasite of its own species. (Jari Peltomäki)

With three distinct types of males, the ruff (Philomachus pugnax) is a strange bird indeed. Now, in a pair of independent papers published Monday in Nature Genetics, scientists have pinpointed the genetic mutations that decide a ruff male's sexual fate.

These three distinct males, each with their own coloring and behavioral quirks, have different versions of one "supergene" -- a region of around 100 genes that come bundled together as a package deal. The males probably diverged from each other over 4 million years ago, and ever since then the three types have existed in a delicate evolutionary balance.

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"The male's reproductive strategy is determined at birth," Terry Burke, a University of Sheffield researcher and an author on one of the two new studies, told The Washington Post.

"Most behavior is flexible. That's the whole point of behavior," Burke said. "But this is predetermined."

This is the first time a set of different types of males -- known as "morphs" -- has been shown to have such a clear genetic root.

The ruff's three types have coexisted for millions of years. The original genome produces what's called an "independent" male, making up 80 percent to 95 percent of the male population. These ruff boys have spectacular plumage, so variable in color as to make each individual look unique. They put all of their energy into gathering together and fighting, making a sort of arena where females can select a mate.

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Then there are "satellite" males, which make up five percent to 20 percent of the population. These males still have plumage, but it's always white. And while they participate in the arena fights, they're always dominated by independent males. Satellite males are actually just biding their time; they carry on their genes by stealing mates already won over by more aggressive birds.

The third type of male is so stealth that researchers only discovered it a few years ago.

"It had been totally undetected, because he looks so much like a female," Burke explained. Indeed, that seems to be the point: The third type, known as "faeder" males, are thought to make up less than one percent of the population. They lack the plumage of other males entirely, and their strategy is to go incognito amongst females of the species. That way they can "steal" mates the same way a satellite male does, while avoiding the violent attention of independent males entirely.

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According to the new findings, the different behaviors are probably caused by differences in the way the birds handle testosterone and other steroids. But the supergene cluster that determines what morph a bird will be also contains genes that control plumage, explaining why behavior and appearance are affected in one fell swoop.

The two research groups who published on Monday came to their conclusions separately.

"It's not so long ago it was very hard work to do a genomic study in any organism," said Leif Andersson of Uppsala University, an author of the second published paper. "The technology has become available now, and it’s such an interesting scientific question, so it's not surprising that two groups were working on solving this riddle at once."

Both Andersson and Burke were surprised to see just how old the genetic variation is.

"The sequence difference is larger than the average sequence difference between humans and chimps, so we estimate it occurred at least 4 million years ago," Andersson explained. 

It wouldn't be unusual for a species to occasionally use different types of mating strategies as needed. But for three kinds of genetically predetermined mating strategies to persist for so long, the researchers explained, they'd have to work together incredibly well. Otherwise, one or both of the alternative male types would have quickly gone extinct, or else replaced the original version entirely.

That's where this evolutionary story gets really cool: The satellite and faeder males actually only have one copy of this modified supergene. Having two copies would be fatal -- probably because of the way the supergene affects the birds' metabolisms.

In this way, the mutation is somewhat similar to sickle cell anemia in humans, where having one copy of a mutated gene gives one an immunity to malaria, while two copies causes a painful, life-threatening illness. Since one copy is very good and two copies are very bad, the mutation has persisted in the population without becoming the norm -- it can never become too prevalent, but it can't disappear because it's too useful.

Being a satellite or faeder male is actually a much better strategy -- you get to pass your genes along without expending as much energy. But the potentially deadly downside of these supergene mutations in birds keep independent males the most common morph. And that's good news for the satellites and faeders.

"In order to counter balance the disadvantage of losing a quarter of your offspring at least, you must be really successful," Burke said. "But they can never be that successful, because they’re kind of parasitic. And to be a parasite, you need enough dominant males to rely on."

If satellites and faeders start to become more common, the benefit of being a mutant starts to drop. That makes them become less common in the population. As these birds become more rare, the advantage of being a parasite goes back up -- and so on and so on, for millions of years.

The delicate dance of these rowdy ruffs, their sneaky satellites and their incognito brothers can now be studied even more closely. Both research teams plan on studying the individual genes inside the supergene cluster in the hopes of determining which mutations are related to the color and behavioral changes we can see in the wild.

"There are over 90 genes, and many of them won't be important," Andersson said. "Exactly what is happening in these birds and how will be very interesting to study."

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