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Evolution: The never-ending story
POSTED 5 FEBRUARY 2009

Don't-call-us, we-won't-call-you: Let's hear it for mute crickets!

Normally, male crickets attract their mates with the summer-night chorus that we might call "natural radio."

But on several Hawaiian islands, crickets have stopped calling, says Zuk. The immediate cause is a mutation that removes the ridges that make the song, leaving "flatwing" crickets. But the ultimate cause is evolutionary: A parasitic fly that has invaded Hawaii locates male crickets by ear, then injects the poor cricket with eggs that form deadly maggots.

Normal and mutant mute crickets

The wing on the mutant male has fine ridges, not heavy, sound-producing ones
Heavy ridges on the wings of normal crickets give that summertime chirping. But when parasitic flies are homing in on the cricket's song, a dramatic mutation eliminates the sound-producing structures among some males.

Guys calling, and females responding, "is pretty basic to your cricketness, and this blew me away in 2003," says Marlene Zuk, a professor of biology at the University of California-Riverside. "I was hearing nothing, but I was seeing crickets in my headlamp. It was astonishing: For a cricket, not being able to call is doom."

She suggests that the silent fellows reproduce by hanging around the few remaining songsters, and mating with the females that he attracts.

In tracing the change to silent crickets, Zuk and her colleagues have focused on one gene mutation that flattens the male's wings. Presumably, she says, the mutation arises commonly under normal conditions, but those males fail to reproduce, so the mutation disappears. But on the island of Kauai, she says, "We had a perfect storm of unusual events that meant that being unable to call was suddenly an advantage."

And that made a rapid difference in the genetics, she has found." The proportion of flatwing males on Kauai increased from 0 to nearly 90 percent in fewer than 30 generations, representing one of the fastest evolutionary shifts documented in a wild population."

The saga of the fly and the cricket exemplifies a struggle between two major evolutionary forces that Darwin discussed:

Natural selection: Better adapted organisms (the silent crickets) will leave more descendants that begin to dominate the population.

Sexual selection: Females make choices that shape the gene pool by increasing the number of singing males.

This struggle appears in studies of wild-collected eggs that are hatched in the lab. Even though normal wings are rare in the wild, they comprise half of the hatchlings, revealing "a tremendous advantage, from a sexual selection standpoint, to being a normal male," Zuk says. But in the fly-infested wild, the scarcity of normal wings "shows there is a tremendous advantage from a natural selection standpoint to being a flatwing."

Chatting with Charles: What would you say to Darwin?

Marlene Zuk: "A lot of things you thought were likely to be true, have come through in ways you could not imagine. You were very interested in behavior, in sex and sexual selection, how sexual differences evolved. I would say, 'That part of your theory is alive and well, and is now interacting with the natural selection part of your theory.'"

What happens next is anybody's guess. "Every time we go back to Hawaii, I think now what?" Zuk admits. If virtually all the crickets go silent, the fly may no longer be able to reproduce inside the crickets, and its population could crash and allow the singing crickets to rebound. But if the last singing male cricket disappears, the mute crickets would die off unless they can find another way to mate.

Lab experiments with crickets show the importance of "social experience," Zuk says. Crickets that grew up hearing adult crickets calling are "a lot pickier about mates. Those that did not hear other crickets are not as fussy about the quality of the song they respond to."

Female crickets in the zone of silence seem to follow a rule of thumb, she adds: Singing males are preferable, but "If there are not a lot of males around, I better take whatever I can get." And this could exemplify a more common interaction between behavior and genetics, she concludes: "We need to look at evolutionary change in the context of the other things the animal is doing."

It's 24/7 evolution in the bibliography!

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Terry Devitt, editor; Nathan Hebert, project assistant; S.V. Medaris, designer/illustrator; David Tenenbaum, feature writer; Amy Toburen, content development executive

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