Key Points
- Hawkmoths have evolved different feeding strategies. While some species have long proboscises they use to drink nectar from specialized flowers, others have short ones that give them access to a wider variety of floral food sources. Some have no proboscises and rely entirely on energy stored during their larval stage.
- In a new study , researchers determined how and when these structures evolved by sequencing DNA and measuring the proboscises of 310 hawkmoth species. The results show that proboscises have repeatedly grown and shrunk over the last 44 million years in response to environmental pressures and latitudinal gradients.
- Hawkmoths have historically been remarked upon by naturalists like Charles Darwin and Alfred Russel Wallace because of an evolutionary arms race that sometimes forms between them and the flowers they rely on for food. As the moths develop longer proboscises to feed on nectar, flowers evolve deeper nectar tubes to ensure the moth continues to pick up pollen, driving both toward an extreme and mutual dependence.
GAINESVILLE, Fla. — Long before his days of research, Christian Couch was just a kid marveling at the butterflies in the Florida Museum of Natural History's Butterfly Rainforest. Years later, after enrolling as an undergraduate student at the University of Florida, that same sense of wonder led him back to the museum, first as a volunteer in the Kawahara Lab and eventually as a master's student studying the insects that first inspired him.
"When I started college, I knew I wanted to volunteer in the Florida Museum because I thought it was a really special place," Couch said. "When I found out I could do research with butterflies and moths, I was even more excited."
Couch recently published the results of his master's thesis in the Royal Society Open Science journal, in which he and his colleagues map out the evolutionary history of hawkmoths. This group is well known for their unusually long proboscises, the strawlike tube that many moths and butterflies use to drink nectar from flowers. One species, Darwin's Hawkmoth (Xanthopan praedicta), has evolved to feed on a particular orchid in Madagascar using a specialized, foot-long proboscis, which is longer than that of any other known species.
But other hawkmoth species have opted for a more measured approach.
"There are different strategies of survival. Some species of hawkmoths have an extraordinary long tongue that is very important for gaining nectar and pollinating the plant, but other hawkmoths have almost no proboscis," said the study's senior author, Akito Kawahara, director of the Florida Museum's McGuire Center for Lepidoptera and Biodiversity.
For Kawahara, the study had been decades in the making. He first set out to conduct the research as a graduate student before ultimately shelving it to focus on other priorities. So, when Couch came along and expressed an interest in hawkmoths, Kawahara was ready with a suggestion.
Hawkmoths and flowers push evolutionary limits
When a moth or butterfly get close enough to a flower for a sip of nectar, it often rubs up against pollen grains that become attached to its scales and proboscises. It advertently serves as a pollinator by depositing a portion of these pollen grains on the next flower it visits.
The relationship between flowers and their pollinators isn't always perfect. Moths have an incentive to get as much nectar as possible, which they can do by evolving a longer proboscis. But, if the proboscis is too long, the moth will stop for a free meal without getting close enough to the flower to pick up the pollen. The flower responds by evolving a longer nectar spur, which prompts the moth to evolve a longer proboscis. Trying to keep up with each other turns into a runaway game of evolution.
"There is a co-evolutionary arms race with the hawkmoth and the flower that has persisted for millions of years. The tongue of the moth becomes longer and longer, and the flower, too, becomes longer and longer," Kawahara said.
Eventually, the relationship can spiral into complete dependence. Long-tubed flowers outgrow all their other pollinators and require an equally matched hawkmoth to do the job. In these cases, the two are so tightly linked that finding one usually means the other is close by.
In 1862, Charles Darwin used this rationale to famously predict the existence of a moth in Madagascar after examining a star orchid (Angraecum sesquipedale) native to the island. This creamy white flower grows high up, tucked among the branches of trees. And most notably, it has an exceptionally long nectar tube. Darwin declared that a moth with a proboscis long enough to siphon nectar out of the plant must exist in Madagascar's forests.
A few years later, naturalist Alfred Russel Wallace seconded the prediction, pointing to several species of hawkmoths with probosces nearly long enough to do the job. It would not be until decades later, in 1903, when scientists finally observed the elusive insect and nearly another century before they observed it feeding on the orchid in 1992.
The incredible tongue of Darwin's hawkmoth is a product of its environment. Hawkmoths found in the tropics tend to have longer tongues than those living in temperate regions. While there is an abundance of plant diversity, these moths often form clear associations with specific plants. This can sometimes mean navigating through dense vegetation to locate those rare compatible host plants where they can lay their eggs. To fuel their journey, they need a lot of nectar. Rather than wasting energy visiting flowers with spurs unsuitable for their long proboscis, the moths use their sense of smell to locate the flowers with nectar tubes that are a match.
Then there are the one-fifth of hawkmoth species that don't have a proboscis at all. The way these hawkmoths have evolved to interact with their environment is strikingly different. Rather than feeding on nectar as adults, these short-lived species rely entirely on the limited energy reserves they pack on during their larval stage. As caterpillars, they tend to be generalists, feeding on a wide variety of plants rather than specializing on just one. This flexibility means the moths don't need to search extensively for a specific host on which to lay their eggs.
And while it is less showy than a foot-long tongue, this generalist strategy is another impressive hawkmoth trait. Most plants produce chemical defenses to deter munching herbivores, yet these caterpillars can feed across a wide range of toxic plant species.
"The ability of hawkmoth caterpillars to tolerate different plant defenses is another thing we still don't understand very well," Kawahara said. "It's remarkable that they can do this across so many different types of plants, even with the various plant chemistries at play."
Tracking the hawkmoth proboscis through time
In this study, Couch and his colleagues were able to trace these various feeding strategies back to their early ancestors. They began by sequencing the DNA of over 300 specimens, which they used to build out a genetic tree that covered about 20% of the world's 1,600 hawkmoth species. With that framework in place, they could examine hawkmoth tongue length to see how feeding behavior changed over time.
To measure each specimen's proboscis, Couch snipped off the coiled tongue of hawkmoth specimens in the museum's Lepidoptera collection, placed it in a relaxing solution and stretched it out to measure with a ruler. Species with long tongues feed as adults, while those with tongues shorter than 0.4 inches are categorized as nonfeeders.
Their results indicate that the earliest hawkmoths did not feed as adults nor do the majority of their closest relatives in the Saturniidae, the wild silk moth family. The first evidence of adult feeding in hawkmoths appears around 44 million years ago. From there, the trait quickly caught on.
"It's not too surprising to have multiple instances where hawkmoths develop this feeding behavior," Couch said. "If a resource like nectar exists, then there's an opportunity for a moth to access it. You would expect this trait to evolve multiple times with the many different ecosystems where this resource exists."
But the path to long-tongued, nectar-guzzling hawkmoths is not linear. Rather than simply cleaving into feeding and nonfeeding lineages, many species appear to have gained and lost the trait multiple times, shifting from nonfeeding to feeding and back. In some cases, this happens within 5 million years, a blip on the evolutionary timescale.
The same environmental pressures that encourage long or short proboscis in the first place can shift to influence the variations in proboscis length over time. Although scientists can't pinpoint specific triggers that cause hawkmoths to lose their long tongues after evolving them, they do have an idea about how the transition can happen so quickly.
Species with long proboscises rely on intricate muscles in their mouths to unroll their tongue and slurp up nectar. But it appears that nonfeeding hawkmoths retain these same muscles, even without functional mouthparts to use them. This underlying anatomy gives the moths an evolutionary head start when conditions shift and it is time to lengthen their tongue once again.
The study was published in Royal Society Open Science.
Paul Masonick, David Plotkin and Jesse W. Breinholt of the Florida Museum of Natural History; Xuankun Li of China Agricultural University; Rodolphe Rougerie of Muséum national d'Histoire naturelle – Paris; Jesse Barber of the American Museum of Natural History and Boise State University; and Ian Kitching of Natural History Museum, London, are co-authors of the study.
