"We think we know a lot about how animals might respond to global warming, but we really have very little idea about their actual genetic response to environmental change," said Hadly, an assistant professor of biological sciences at Stanford.

In the study, she and her colleagues conducted a genetic analysis of two species of rodents commonly found in Wyoming's Yellowstone National Park � the montane vole (Microtus montanus) and the northern pocket gopher (Thomomys talpoides).

The researchers collected DNA from living animals and from the teeth of fossilized specimens whose remains were buried in Lamar Cave, a remote site near the northeast entrance to the park.

"The deposit in the cave is about nine yards deep and it took me seven years to excavate and identify the fossils," Hadly said.

"It contains hundreds of thousands of bones and represents a continuous fossil record dating back 3,000 years. This timescale allows us to really investigate microevolution in a natural environment, the way you'd investigate it in a laboratory with something that has a much quicker generational timeline, such as bacteria or fruit flies."

Climate change and genetics

For the experiment, the research team compared DNA from voles and pocket gophers living near Lamar Cave with ancient DNA from fossilized rodents that inhabited the area at different times since 1000 B.C.

The researchers were particularly interested in animals that were alive during two recent climatic events � the Medieval Warm Period (850-1350 A.D.), when the Northern Hemisphere experienced a slight warming trend; and the Little Ice Age (1350-1950), when the hemisphere cooled.

Since voles and pocket gophers prefer relatively wet grasslands, the scientists expected to see a decline in the population of both species during the Medieval Warm Period when their habitats dried up, and an increase during the Little Ice Age when the climate was wetter.

That prediction was confirmed by an analysis of fossil abundance in Lamar Cave, which revealed a 40 percent drop in the vole population during the warmer period, along with a 50 percent decline in the number of pocket gophers.

As expected, fossil abundance for both species rose dramatically during the Little Ice Age as precipitation levels increased.

These findings established a direct correlation between climate change and population size, but how did individual voles and pocket gophers respond genetically to these episodes of global warming and cooling?

Earlier studies have shown that, when an isolated population shrinks, inbreeding increases. As a result, surviving offspring end up with similar DNA.

Over time, this lack of genetic diversity can jeopardize the entire population, because each individual inherits the same vulnerability to diseases and other external threats.

"When you decrease population size, you have the potential of eliminating much genetic diversity," Hadly explained.

"That's what happened to pocket gophers during the Medieval Warm Period. We found that they underwent a population size reduction and a decline in genetic diversity, which is what you would predict."

But voles had a different response to medieval warming. "They didn't show any reduction in genetic diversity, even though they did show a reduction in population size," Hadly said. That's because voles routinely look for mates from other colonies.

"Voles move around," Hadly noted. "They disperse quite freely, and that actually results in an elevation of genetic diversity during the time that their population sizes are undergoing reduction. Pocket gophers, on the other hand, are subterranean rodents. They dig underground burrows that are very energetically expensive to build, and they kind of stick in one place."

Subtle message

These results have important implications for wildlife biology and conservation, Hadly observed.

"There's a subtle message in this paper about the potential influence of warming on evolution," she said.

"Voles show an influx of new genes and genetic diversity as their population declines, which means they're connected to other populations. But gophers haven't really recovered from the Medieval Warm Period, which ended less than 1,000 years ago. That means gophers are not getting any fresh, new genes from somewhere outside because they're isolated."

While previous studies have shown that interbreeding usually occurs among large populations of animals, "this study shows that gene flow is occurring when population sizes are low," Hadly said.

"So the snapshot we have today about how populations are connected may not be how it actually persists through time."

The study also has implications for wildlife managers in the greater Yellowstone ecosystem who are trying to maintain genetically diverse populations of elk, bison and other mammals.

"The landscape of Yellowstone � arguably one of the largest relatively intact temperate zone ecosystems in the world � is really chopped up and isolated, and there are fewer connections between populations," Hadly explained.

"They really might not have anyplace to go because of development or habitat loss, and this has the potential to be exacerbated during global warming."

She noted that the methods developed for the study offer wildlife biologists a unique approach to understanding the long-range effects of climate change on genetics.

"In looking at wild organisms in nature, I don't really know of another study like this," she said.

"No one has really looked specifically at how the environment has influenced genes over a 3,000-year timescale. And our expectation is that other species will also show genetic responses to warming. Whether these effects are reversible may have to do with life history and how connected populations are, and for many species that remains to be seen."

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