Crickets on Hawaiian Island develop silent wings in response to parasitic attack

In only a few generations, the male cricket on Kauai, one of the Hawaiian Islands, underwent a mutation – a sudden heritable change in its genetic material – that rendered it incapable of using song, its sexual signal, to attract female crickets, according to a new study by UC Riverside evolutionary biologists.

In addition, the researchers found that although the new male crickets' wings lack the file and scraper apparatus required for producing sound, the males are able to mate successfully with females, thus ensuring evolutionary success. They accomplish this by simply altering their behavior in an ingenious manner, suggesting that behavior can help what may seem like a harmful mutation spread.

The research team, led by Marlene Zuk, a professor of biology, found that greater than 90 percent of male field crickets (Teleogryllus oceanicus) on Kauai shifted in less than 20 generations from having normal wings to mutated “flat wings” that inhibit the crickets from calling. The mutation occurred, the researchers conclude, to protect male crickets from a deadly parasitic fly (Ormia ochracea) that uses the cricket song to locate crickets as hosts.

Upon finding a male cricket, the fly deposits larvae onto it; these then burrow into the cricket, develop inside, and subsequently kill the cricket when they emerge from its body. Of three Hawaiian Islands (Oahu, the Big Island of Hawaii, and Kauai) where the cricket and fly co-occur, Kauai, where the rapid spread of this wing mutation in male crickets was observed, has the highest prevalence of the parasitic fly.

Study results appear in Biology Letters, a scientific journal of the Royal Society in the United Kingdom, publishing short papers from across the biological sciences.

“With each visit we made to Kauai since 1991, we observed fewer crickets,” said Zuk, the first author of the paper. “In 2001, we heard only one calling male. But then in 2003, although we heard none of the male crickets calling, we found they were not only in high abundance but nearly all of them also had female-like wings, lacking the fine structures needed to produce song.”

The researchers also found that male cricket populations in Oahu and the Big Island, as well as descendants from eggs collected on Kauai before 2003, continued to show normal wings. Only on Kauai were the mutated wings seen in male crickets in 2003.

“Loss of calling clearly seems to be protecting the male crickets from the deadly fly,” Zuk said. “But this protection has a heavy price: the loss of its sexual signal. This is obviously a huge loss for the cricket, akin to, say, finding that all peacocks in a forest have lost their tails. One might ask how then do female crickets locate silent flatwing males?”

Zuk and colleagues propose that on Kauai, the flatwings – a term they use to identify male crickets with mutated wings – behave as 'satellites' to the few remaining male crickets that can call. By congregating near the callers, the flatwings enable females to find and mate with them.

To test their hypothesis, the biologists performed a field experiment that demonstrated that the flatwings are using the callers as female attractors (for details, see below).

“While we were surprised by the extraordinary speed at which the mutation spread, what is more interesting is that, ordinarily, you would expect such a change in wing morphology to quickly disappear, because males couldn't attract mates,” Zuk said. “Instead, the behavior of the flatwings allows them to capitalize on the few callers that remain, and thus escape the fly and still reproduce. This is seeing evolution at work.”

Field experiment details:

The researchers performed experiments in which 2-meter radius circles were delineated within the habitat of crickets on Oahu, the Big Island of Hawaii, and Kauai. After removing and noting the sex, the wing type and the number of all crickets inside the circle, the researchers played an island-specific calling song from a speaker placed in the circle's center. After 20 minutes, the researchers noted the position, sex and wing structure of all crickets inside the circle, and measured the distance from all crickets to the speaker.

Comparing their observations made on the three islands, the researchers found that on Kauai, the flatwings arrived much more quickly, and settled closer to the speaker, than normal-winged males on the other two islands, supporting the notion that the new morphs are using the callers as female attractors.