From Squeaks to Song

FLICKR, DULLHUNK Dustin Penn eats, sleeps, and breathes sexual attraction. An evolutionary biologist at Vienna’s University of Veterinary Medicine, he studies the intricacies of courtship, focusing on those biochemical signals that help animals choose their mates. He’s studied them in songbirds, zebrafish, and humans—but his species of choice is the house mouse, Mus musculus. Surrounded by cages in his lab, Penn has spent years hearing mice unmelodically squeak and chirp in the background as he worked to understand how they use smell to identify their mates. So when he first learned that male mice vocalize in the presence of females—singing, out of the range of human hearing, true songs that transcend the randomness of squeaks—he nearly flipped his lid. “House mice are one of the most extensively studied organisms on the planet, and they sing like birds, and we don’t know anything about how it’s evolved or their behavior,” Penn says. Despite specializing in the hormonal aspects of behavior, he dove right in, figuring that “after chemical signals, acoustic signals are an interesting place to go.” Up to that point, studies of ultrasonic mouse singing had been conducted exclusively in lab mice. Reasoning that the years of breeding for other traits might interfere with the songs’ melody and function, Penn went into the field to collect wild mice for his experiments. He recorded the males’ songs and played them back for females to see whether they’d respond. And they did: wild female mice were attracted to the tune of the murine Sinatras, preferentially hanging out in front of the speaker playing the vocal tracks (Anim Behav, 79:757-64, 2010). IN TUNE: The experimental arena Penn used to test female mice’s attraction to male singing. FRAUKE HOFFMAN The females also lapped at their fur, preening themselves, while listening to adult male mice sing. But they stopped the behavior when their brothers’ songs were played, even though they had never heard their brothers sing in the flesh. “This suggested that the songs were used for distinguishing kin from non-kin,” says Penn. “What we want to know now is what the females are doing with this information. Can it help them identify better-quality mates?” Charlie Walcott, a Cornell University ornithologist who studies birdsong, was surprised that he and the bird community had not yet heard of the singing mice, especially considering how similar the functions of each species’ song appeared. “The whole idea for a birdsong is to say, ‘Here I am, I’m a male songbird; if you’re a female I’d love to get acquainted, and if you’re a male I’ll pull your feathers out!’” he says. The mouse song “certainly has to do with attracting females, and the playback experiments make that quite clear. The question that I have is: What about male-male interaction?” Penn hasn’t delved into whether the songs are used as signals of male-male aggression, but he has started picking apart the differences in song structure. Using the same software used to analyze birdsong, he compared the songs among brothers and between unrelated mice. The brothers’ songs were very similar—and previous work in lab mice suggested that the melodies are innate—but each also expressed distinct individuality (Physiol Behav, 105:766-71, 2012). These vocal “fingerprints” could be used to help mice tell one another apart, Penn says, and he plans to look into it. Spectrographic analysis of the vocalizations also presented a fresh opportunity to scrutinize whether they really should be described as songs or just as patterned squeaks. “If they weren’t up there so high” in the ultrasonic frequency range, “I wouldn’t know that they weren’t birdsongs,” says Pam Rasmussen, an ornithologist at Michigan State University. “There’s so much we don’t know about groups we think we’re familiar with.” Although mouse songs haven’t quite taken the ornithological community by storm, people who study the mouse brain are all ears. Neurobiologist Tim Holy, who published the 2005 paper that inspired Penn (PLoS Biol, 3:e386), hasn’t personally touched mouse-song research since. But his postdoc Terra Barnes at Washington University in St. Louis picked up where he left off. Using mice that are genetically modified to sing a disrupted song, she is trying to model stuttering, and she says other researchers are using the mice to better understand neurological diseases. “A lot of really good research has been done in birdsong as it relates to the basal ganglia,” the region of the brain associated with speech disorders as well as diseases such as Parkinson’s and Huntington’s, Barnes says. However, bird brains are quite different from mammalian brains. “If we could join the two fields, taking what’s been learned in birdsong and applying it to mouse song, that would be really cool.”

From Squeaks to Song

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May 2012

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