How hawkmoths turned their genitals into bat-busting weapons

When a bat closes in, some hawkmoths fight back with their genitalia. By rasping specialized scales on their sex organs against structures on their abdomens, the moths unleash bursts of ultrasound that can scramble the sonar a hungry bat uses to lock onto prey.

But this acoustic counterattack is no evolutionary one-off. Relentless pressure from predators has pushed these otherwise tasty insects to reinvent this defensive tactic up to seven times throughout their evolution, with separate lineages arriving at distinct anatomical solutions to the same threat, researchers report November 4 in the Proceedings of the Royal Society B.

The findings suggest that the high-frequency acoustic skirmishes playing out overhead each night, beyond the range of human hearing, may be far more varied than scientists realized.

“Clearly the hawkmoths as a whole have more tricks up their sleeve,” says Marc Holderied, a sensory biologist and bioacoustics researcher at the University of Bristol in England who was not involved in the study.

The discovery builds on more than a decade of research by sensory ecologist Jesse Barber, now at the American Museum of Natural History in New York City, and entomologist Akito Kawahara of the Florida Museum of Natural History in Gainesville. Those scientists’ earlier work showed that moths across multiple families, from tiger moths and fruit-piercing moths to geometer moths and jewel caterpillar moths, produce ultrasound in response to bat attacks. Other insects, including some beetles and fireflies, do too.

But among the most striking defenders are hawkmoths, a family of some 1,600 mostly nocturnal, torpedo-shaped speedsters, also known as sphinx moths, that hover at flowers like hummingbirds. Many fend off bats by scraping their genitalia like a fingernail dragged along a comb, producing ultrasonic clicks that can disrupt the predators’ sonar.

The anatomical diversity of these sound-producing systems, however, and how they evolved remained poorly understood. So Barber, Kawahara and their team, including Florida museum colleague and evolutionary biologist Paul Masonick, combined audio recordings of male hawkmoths responding to bat calls with high-resolution imaging of preserved specimens from overlapping species. Although some females also produce ultrasound, the researchers focused on males because female sound creation remains too poorly documented for systematic analysis.

Among the 143 species tested, 77 produced ultrasound. They did so in three distinct ways. All three rely on a patch of enlarged, football-shaped scales on the male’s genital valves, which are paired structures used to clasp females during mating. But what those scales scrape against varies.

Some rub the scales against a row of corresponding scales near the rear of the abdomen. Others drag them across stiff spines jutting from the abdomen’s edge. Still others rasp them over a field of microscopic bumps on the insect’s underside, a previously unidentified part of the sound-making apparatus.

These mechanical differences are reflected in the sounds themselves. Moths that scrape their genital scales against spines or tiny bumps tend to make more continuous noise, with greater potential to jam bat sonar. Those that scrape scales against other scales produce irregular bursts, which may startle attackers or mimic the warning calls of foul-tasting prey.

Notably, moths that scrape against the newly identified bumpy surface have the broadest acoustic repertoire, with even close relatives sounding quite different. That flexibility could give them more options for evolving new defenses against bats, notes Nick Dowdy, an evolutionary biologist at the Milwaukee Public Museum who was not involved in the research. Other groups, by comparison, may be more constrained by their anatomy, he says, leaving them “locked into certain strategies.”

The authors estimate that genitalia-enabled ultrasound production evolved independently at least four and as many as seven times between roughly 5 million and 30 million years ago. According to Masonick, it is a vivid example of convergent evolution in which the same predatory menace repeatedly drove the moths to adapt similar behaviors through different anatomical routes.

But the evolutionary arms race was not a one-way street, he points out. Several hawkmoth lineages that shifted toward twilight or daytime activity subsequently lost their specialized sound-producing machinery.

“It goes to show how intense bat predation is on insects,” Masonick says. “It’s been a major driver of insect evolution.”