Fruit, nectar, bugs and blood: How bat teeth and jaws evolved for a diverse dinnertime

They don't know it, but Darwin's finches changed the world. These closely related species -- native to the Galapagos Islands -- each sport a uniquely shaped beak that matches their preferred diet. Studying these birds helped Charles Darwin develop the theory of evolution by natural selection.

A group of bats has a similar -- and more expansive -- evolutionary story to tell. There are more than 200 species of noctilionoid bats, mostly in the American tropics. And despite being close relatives, their jaws evolved in wildly divergent shapes and sizes to exploit different food sources. A paper published Aug. 22 in Nature Communications shows those adaptations include dramatic, but also consistent, modifications to tooth number, size, shape and position. For example, bats with short snouts lack certain teeth, presumably due to a lack of space. Species with longer jaws have room for more teeth -- and, like humans, their total tooth complement is closer to what the ancestor of placental mammals had.

According to the research team behind this study, comparing noctilionoid species can reveal a lot about how mammalian faces evolved and developed, particularly jaws and teeth. And as a bonus, they can also answer some outstanding questions about how our own pearly whites form and grow.

"Bats have all four types of teeth -- incisors, canines, premolars and molars -- just like we do," said co-author Sharlene Santana, a University of Washington professor of biology and curator of mammals at the Burke Museum of Natural History & Culture. "And noctilionoid bats evolved a huge diversity of diets in as little as 25 million years, which is a very short amount of time for these adaptations to occur."

"There are noctilionoid species that have short faces like bulldogs with powerful jaws that can bite the tough exterior of the fruits that they eat. Other species have long snouts to help them drink nectar from flowers. How did this diversity evolve so quickly? What had to change in their jaws and teeth to make this possible?" said lead author Alexa Sadier, an incoming faculty member at the Institute of Evolutionary Science of Montpellier in France, who began this project as a postdoctoral researcher at the University California, Los Angeles.

Scientists don't know what triggered this frenzy of dietary adaptation in noctilionoid bats. But today different noctilionoid species feast on insects, fruit, nectar, fish and even blood -- since this group also includes the infamous vampire bats.

The team used CT scans and other methods to analyze the shapes and sizes of jaws, premolars and molars in more than 100 noctilionoid species. The bats included both museum specimens and a limited number of wild bats captured for study purposes. The researchers compared the relative sizes of teeth and other cranial features among species with different types of diets, and used mathematical modeling to determine how those differences are generated during development.

The team found that, in noctilionoid bats, certain "developmental rules" caused them to generate the right assortment of teeth to fit in their diet-formed grins. For example, bats with long jaws -- like nectar-feeders -- or intermediate jaws, like many insect-eaters, tended to have the usual complement of three premolars and three molars on each side of the jaw. But bats with short jaws, including most fruit-eating bats, tended to ditch the middle premolar or the back molar, if not both.

"When you have more space, you can have more teeth," said Sadier. "But for bats with a shorter space, even though they have a more powerful bite, you simply run out of room for all these teeth."

Having a shorter jaw may also explain why many short-faced bats also tended to have wider front molars.

"The first teeth to appear tend to grow bigger since there is not enough space for the next ones to emerge," said Sadier.

"This project is giving us the opportunity to actually test some of the assumptions that have been made about how tooth growth, shape and size are regulated in mammals," said Santana. "We know surprisingly little about how these very important structures develop!"

Many studies about mammalian tooth development were done in mice, which have only molars and heavily modified incisors. Scientists are not entirely sure if the genes and developmental patterns that control tooth development in mice also operate in mammals with more "ancestral" sets of chompers -- like bats and humans.

Sadier, Santana and their colleagues believe their project, which is ongoing, can start to answer these questions in bats -- along with many other outstanding questions about how evolution shapes mammalian features. They're expanding this study to include noctilionoid incisors and canines, and hope to uncover more of the genetic and developmental mechanisms that control tooth development in this diverse group of bats.

"We see such strong selective pressures in these bats: Shapes have to closely match their function," said Santana. "I think there are many more evolutionary secrets hidden in these species."

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Whiskers help nectar-eating 'acro bats' hover like hummingbirds

From dragonflies to hummingbirds, hovering flight is among the most complex and captivating forms of animal movement -- a physiological feat of size, musculature and wing development.

For nectar-feeding bats that hover as they feed from flowers, this aerial maneuver also depends on extra-long whiskers unlike those of most other bat species, according to a Dartmouth College-led study in the journal Proceedings of the Royal Society B. The researchers used high-speed cameras to capture how the stiff hairs jutting forward from the face of nectar-eating bats provide enhanced spatial information that guides the animals as they swoop in to quickly feed -- within a second or less -- on succulent flowers without landing.

"The whiskers of nectar-feeding bats are critical sensory organs that provide high-quality input the brain works with to optimize hovering. It's a cool junction between sensory biology and bio-kinematics, between form and function," said lead author Eran Amichai, a postdoctoral researcher in biological sciences at Dartmouth who studies echolocation in bats. Co-authors are postdoctoral fellow David Boerma from the American Museum of Natural history, animal behavioralist Rachel Page at the Smithsonian Tropical Research Institute in Panama, Sharon Swartz, a professor of biology and engineering at Brown University, and Hannah ter Hofstede, a past assistant professor of biological sciences at Dartmouth now at the University of Windsor in Canada.

The researchers worked at the Smithsonian Tropical Research Institute recording Pallas's long-tongued bats -- a South and Central American bat that has the fastest metabolism of any mammal -- as they drank from hand-blown glass flowers designed for the study to replicate the plants the animals feed from. High-speed infrared cameras captured photos and video of the bats as they descended upon the glass flowers and navigated their muzzles and tongues into the "bloom" to eat the nectar. Feedings typically lasted between a half- to one second.

The researchers found that bats with clipped whiskers were less agile and accurate during feeding and flight than animals with untouched whiskers. The animals with clipped whiskers were held for a few days until the hairs regrew, then released back into the jungle. "Clipping the whiskers doesn't reduce the bats' ability to feed, they just do it a little less gracefully," Amichai said. "If it were gymnastics, they'd get an 8.5 instead of a 9.8."

The role of long whiskers in nectar-feeding bats' flight control provides new insight into the coevolution of the bats with the flowers they feed on, Amichai said. The majority of bats possess short whiskers not arranged in any particular pattern or direction. But the researchers found that whisker length in nectar-eating bats evolved at least twice to -- along with long tongues and faces -- potentially help them better navigate the deep chambers of the flowers they prefer. In turn, the long reach these flowers require results in more pollen sticking to their pollinators and thus the broader proliferation of their kind.

The researchers plan to continue their work using higher-resolution images, flowers that move, interactions with predators and other expansions on the experimental model, Amichai said.

In the meantime, the latest study offers a fascinating glimpse into how nectar-feeding bats combine various forms of sensory information to navigate the world around them, Amichai said. Their world is a combination of scent, echolocation, spatial memory, knowledge of the seasons and the physical sensation and equilibrium provided by their whiskers.

"I find thinking in these terms of switching back and forth between completely different ways to perceive the world -- and seamlessly integrating their input -- to be a mind-blowing concept," Amichai said. Understanding how animals perceive and interact with their surroundings helps scientists develop better conservation strategies, he said.

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