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Robin Tinghitella (center) and her fellow researchers pose for a photo while working at a table in Hawaii.

����ֱ�� Associate Professor Robin Tinghitella is dissecting the hidden world of animal communication, where eavesdropping parasitoid flies influence how crickets sing and, ultimately, how they survive.

Tinghitella’s latest research, published in the journal��, has made progress in understanding how eavesdroppers, animals that secretively listen in on the communication of other species, impact how the animals they are listening to talk to one another.

Specifically, she and her colleagues found that the Hawaiian parasitoid fly Ormia ochracea—whose larvae live inside of and feed on a host insect, the Pacific field cricket—has evolved to better detect the cricket, creating an evolutionary arms race of sorts. Both the fly’s hearing and its behavior is what the behavioral ecologist calls “evolutionarily labile.”

When male crickets sing, they attract intended receivers, such as a mate, and unintended receivers, like a predator or parasitoid that uses the signals to locate a host or prey they plan to kill, Tinghitella says. Over time, the crickets’ songs changed to avoid predators.

“The interaction between the cricket and the parasitoid fly is something that people have known about in Hawaii for about the last 35 years, but this is the first time that we’ve ever detected reciprocal evolution on the part of the fly to keep up with changes that are happening in the cricket,” she says.

Tiny treadmills and campus lawns

Tinghitella’s research is conducted in Hawaii, but not along the sandy beaches or in the lush jungle environment that might first come to mind.

You would instead find Tinghitella and her team in the laboratory or situated on the grassy lawn of Brigham Young University-Hawaii in Oahu.

“(The crickets) live on lawns. So instead of field work, we often joke in the lab that we do lawn work,” she says.

Two of the three experiments, which looked at the fly’s neural and behavioral responses, were completed in the lab.��

To understand the neural responses, researchers placed an electrode into the fly’s neck connective, a bundle of nerve fibers where auditory neurons relay auditory input to the brain and then broadcast sound pulses, Tinghitella says.��

The fly’s behavioral responses were recorded using what is essentially a mini treadmill for insects. Researchers affixed a tether to the fly using wax and then placed it on top of a lightweight ball that floated above a constant airstream, she explains. Researchers played different cricket songs and, when the fly walked or ran, the ball rotated and a laser pointed at the ball captured movement, indicating the fly was reacting to the sound.��

The field work, which was conducted on the campus lawn in Hawaii, involved setting fly traps where researchers knew crickets and flies would co-occur and playing various songs inside the traps to see if the flies were drawn inside. One thing they discovered was that the flies are drawn in by new cricket songs only at relatively close distances.

‘Being in the right place at the right time’

Tinghitella says one of the greatest challenges in studying the evolution of animal communication systems is “being in the right place at the right time.”

Back in 2017, Tinghitella discovered the first novel cricket song, referred to as the purring song. That was the first time that the evolution of a new animal signal had ever been directly observed in nature, she says.

“Never before had anyone seen this kind of thing happen. So, this is a once in a lifetime opportunity, to not only get to see these novel signals evolving but to study in real time how that impacts the animals that are using those signals,” Tinghitella says.

Another challenge with this type of research is the amount of time it can take to collect “what feels like one data point.” Tinghitella says it can sometimes take an entire day to dissect the fly, place the electrode, conduct all the tests, including playing hundreds of sound pulses, and record the data.

The next step in Tinghitella’s research includes work on a separate but related longitudinal study she leads, where her team goes out to Hawaii every six months to continually track in real time what these evolutionary interactions look like.

She’s also particularly interested in the role female crickets play in all of this.

“Communication is a really tight-knit relationship between, in this case, intentional communication between male crickets that are producing songs and female crickets that receive those songs and use them to make decisions about who they're going to mate with,” she says.

Female crickets in Hawaii are unique in that they are willing to accept males who produce diverse and novel songs. In any other location in the world where these crickets exist, if the songs had evolved, they would be “selected against” by very choosy females, she says.

“So, we’re really interested in understanding what has led to this broad acceptance of different types of males in Hawaii, and why is it that female behavior is different and is facilitating this new evolution of song,” Tinghitella says.