Research

How do signals used in mating evolve?

Many animals use bright colors, songs or odors to attract potential mates, and scientists have spent a lot of time examining the behaviors that favor particular signals. In most species, it’s the males that produce the signals while the females choose their mates.

All of those signals share an important characteristic: they are conspicuous, which makes sense in the context of mate attraction. But that conspicuousness can also make the signaler easier to detect by potential predators and parasites, as occurs when bats use frog calls to locate prey:

My research centered on a similar case of signal exploitation, in crickets that are parasitized by a fly that hears male crickets chirping, homes in on them, and deposits larvae that burrow inside the cricket and eat him from the inside out while he’s still alive. Gory!

Here’s what the fly and cricket look like:

And here’s the fly maggot emerging from the cricket, followed by a photo of a dissected male cricket with several maggots inside:

This gruesome situation raises many questions. Males face a conundrum because singing is beneficial, even essential, because it attracts females, but is can also be deadly. How do they (evolutionarily speaking) deal with this dilemma? I spent several decades studying how these conflicting selection pressures are worked out in Teleogryllus oceanicus, the Pacific Field Cricket, which is native to Australia and many Pacific islands. It was introduced to Hawaii by humans, where it is subject to being attacked by one of those parasitic flies, Ormia ochracea. Other than in Hawaii, the flies are absent and the crickets can sing in peace, which means we have a kind of natural experiment of how the crickets respond to the parasitic flies.

My students, postdocs and I studied the situation for many years, and you can find out much more on my lab website as well as look up all of our publications on my Google Scholar page. Feel free to contact me for more information, too.

Some of the highlights:

Crickets in Hawaii show modifications in their songs that make them less apparent to the fly. 

We surveyed songs in several populations with and without the parasites, and found consistent differences in the parasitized population. Problem is, those differences also make the males harder for females to find.

Some normal-wing males remain in populations with the flatwing, and we think that a kind of push-pull of evolution keeps both types viable.

The idea is that when flatwings are abundant, they have more offspring. That in turn means that the calling males, which are preferred by females, have a big advantage, so they then produce a disproportionately high number of babies. That then favors the flatwings because the calling males are susceptible to the flies, and are more likely to die.

The flatwings showed us how pre-existing flexibility in behavior can help a completely new characteristic get established.

Flatwings don’t get parasitized, but what about mating? We found that the female crickets from islands, including Hawaii but also Tahiti and Samoa, were more receptive to males that couldn’t sing than were females from mainland populations. This greater tolerance may occur because island populations experience less selection on females to be picky.

We saw evolution in action on the Hawaiian island of Kauai with the emergence of a new morph of males that cannot sing.

Crickets call by rubbing their wings together, making sound a bit like the way you can produce noise running your fingernail across a comb. My colleagues and I had been working in Hawaii since 1991, but in 2003 we discovered something completely unexpected: a new kind of male appeared, with wings that lacked the distinctive structures needed for singing. We call them “flatwings,” and we found that they are completely protected from the fly. The altered appearance is caused by a single sex-linked gene, and it spread throughout the population in fewer than 20 generations, an evolutionary blink of an eye.

Here’s an electron microscope photo of the difference in the wings (females never sing, and always lack the special structures):

Other Projects & Interests

Over the years, I’ve also studied the evolution of sex differences in disease susceptibility, how parasites affect host behavior, same-sex behavior in animals, and some really bizarre crickets called lava crickets. The latter live, logically enough given their name, on barren lava fields on the Big Island of Hawaii, and are fascinating because they can persist where few other living things can. They spend their time deep in the cracks and emerge at night to feed on detritus that blows in from the surrounding area. They are wingless, which means that the males can’t sing like other crickets, bringing up the question of how males and females find each other in the vastness of the lava fields.

Here are a few photos of the environment; it’s an amazing place to work but very rugged:

This is me at the Mauna Ulu site in Volcanoes National Park

And me with former postdoc Justa Heinen-Kay.

This one is self-explanatory.