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Climate Change Genomics Heats Up

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Earth scientists and environmentalists have been sounding warnings for years that climate change is going to do permanent harm to the Earth. At a conference in London in March, Reuters reported even more dire warnings from climate scientists, who cautioned that the rise in the world's temperatures is close to reaching the point where the effect on the environment will be irreversible. Will Steffen, executive director of Australian National University's Climate Change Institute, called this the "critical decade," Reuters said. "If we don't get the [temperature] curves turned around this decade we will cross those lines," Steffen added.

For many years, earth scientists have been studying the effects of climate change — both natural temperature changes and human-made environmental problems — on animals, plants, microbes, and ocean life. Now, genomics researchers are getting interested in climate change, working with their counterparts in the environmental sciences to determine whether there is a genetic basis for the responses of various living organisms to environmental upheaval.

"A big question about the fate of species given climate change is what species are going to be able to survive, and survival's going to depend on a species' or individual's ability to compensate for changes in the environment," says the University of California, Davis' Andrew Whitehead.

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In an article published in the Journal of Experimental Biology in March, Whitehead wrote that modern functional genomics approaches and technologies offer researchers an opportunity for a more refined understanding of the genetic -basis of an organism's response to its environment. "What genomics techniques can do is advance our understanding of how the structure of your genome is related to your phenotype, your physical abilities, or your morphology, or your behavior. So it's really advanced our ability to link that genetic background with your phenotypic abilities," he says.

It is this link between a species' phenotype and genotype — its ability to evolve traits that will serve it well in a new environment or at a different temperature — that Whitehead says genomics researchers can help elucidate. "When you're able to sequence the genetic makeup of an individual or population or species, you can start to look for differences that might explain their different evolved abilities," he adds. "And then by doing functional experiments where you're looking at what genes are turned on or turned off in different environments — and looking at that in different species — that pushes you much further forward in understanding what mechanisms, what biochemical pathways, are mobilized in one species' response to the environment."

Time to move

Researchers already know that humans can adapt their physiology to fit their environment. That's how people are able to populate almost any kind of terrain, Whitehead says. But not all species have such broad adaptive abilities. "The species that are able to adjust will be able to adjust without having to do much," he adds. "Other species have got more hard limits on what their physiology can do under different environmental limits. So to persist, those species are going to have to move to a more appropriate habitat."

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A team of researchers at the University of Bristol is studying the genome of the British butterfly Aricia agestis, searching for evidence of an evolutionary response to climate change. What they've found thus far suggests that evolutionary changes, which corresponded to a range expansion, correlated with rising temperatures in the butterfly's habitat. As the areas where the butterfly lives have warmed, some populations have moved short distances north. The study, which was published in Molecular Ecology in November, showed that as the butterflies move into new areas, they adapt to new habitat types — including new host plants — drawing on variation that already exists within their genomes to adapt, says first author James Buckley, who is now at the University of Glasgow.

The team conducted an amplified fragment length polymorphism-based genome scan on the butterflies and used outlier-based and association-based statistical techniques to identify loci associated with the organisms' range expansion. About 5 percent of the AFLP loci are associated with the butterflies' range expansion and use of new habitat, the team concluded. "They're basically using pre-existing variation for habitat use or habitat preference, and that's under selection, as they move into new areas," Buckley says. The team also found evidence of new loci related to range expansion, as the butterflies moved to colonize new areas.

"We weren't necessarily surprised, but we were interested to see that there is selection on existing variation genetically," he adds. "And there is strong evidence that there is evolutionary change in other traits as well. That's really exciting because it does mean that only a subset of individuals are best able to colonize new areas." The team has ongoing transcriptomic work with the butter-flies, using Roche 454 sequencing to characterize the transcriptome to explore whether different genes are expressed in different populations.

The organisms within

But it is not just climate change that affects natural environments, and it is not just species' genomes that researchers are studying. Some researchers are concentrating their efforts on how organisms respond physiologically to human encroachment on their environment. For example, Davis' Whitehead says, some researchers study how birds have evolved to be able to sing at higher frequencies, so they can communicate over the din of big cities.

At the University of Illinois at Urbana-Champaign, Carl Yeoman conducted a study of black howler monkeys in Mexico, looking in particular at how the loss of their natural environment affects their microbiomes, and in turn, their health.

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"From our perspective, we're looking at microbial changes as they relate to the gut invasional system," Yeoman says of that work, which he presented at the Association of Biomolecular Resource Facilities annual meeting held in Florida in March. "Genomics technologies are fundamental to achieving that, given that the vast majority of microbial biodiversity cannot be cultured using traditional techniques."

The researchers examined five groups of howler monkeys. Two groups occupied their natural habitat — a continuous evergreen rainforest, in Palenque National Park in the Chiapas state of Mexico. A third group lived in a fragment of rain-forest on the outer edges of the park. A fourth group lived in a semi--deciduous forest about 200 miles from the park. And the fifth group lived in captivity. The team collected fecal samples over the course of eight weeks, extracted the DNA, and sequenced it using 454, aiming for about 10,000 sequences per sample.

In keeping with the different environments, the monkeys had different resources. The researchers found that the howlers in the pristine rainforest environment targeted different plants and different parts of the plant — the flowers and fruit — than the howlers in the semi-deciduous forest, which targeted mostly leaves. The captive monkeys ate mostly Monkey Chow.

The available resources affected the howlers' gut ecologies in different ways, Yeoman says. "Despite a more varied diet among individuals of the pristine continuous evergreen rainforest, the compositions of their microbiomes are much more similar in terms of what bacteria are there," he says. "In contrast, those occupying the semi-deciduous forest have a more similar diet among individuals, but there is more individual variation in what bacteria are detected in their feces. This suggests the microbiomes of the semi-deciduous forest group are less stable."

When the team looked at alpha-diversity — the number of different microbial species within an individual — to gauge the difference in microbial types within individual howlers, they found a loss of diversity in the groups living outside the pristine rainforest environment, getting less and less diverse the further the monkeys were from their natural habitat. "This is significant because ecological theory — supported by experimental evidence in environmental and host-associated microbial ecosystems — points to a loss of richness and diversity as a weakening or perturbation of that ecosystem," Yeoman says. "Basically it is believed a rich microbiome with high diversity should be capable of fulfilling more functions, and even be functionally redundant, and so be more resilient to being perturbed."

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Indeed, the howlers with the least alpha-diversity — those in captivity — died within six months of sampling. "In every case that we've looked at, when you compare primates within wild environments to primates in captivity, they're completely different, and they lose diversity in captivity — that's in terms of who's there and in terms of the functional gene content as well," Yeoman adds. This would indicate that human-made environmental problems, like the loss of a natural rainforest habitat, would negatively affect at least this species of primate through a perturbed microbiome.

Yeoman's team will do a longer term study of the howlers. His team has already collected fecal samples from the animals over the course of nine months, and plans to see if the microbiome perturbations continue. In addition, Yeoman says, upon moving to Montana State University in a few months, he wants to do similar studies in Yellowstone National Park and "other ecologically interesting sites."

Moving forward

The literature on the genomics of climate and environmental change is sparse, as yet. But more and more researchers are doing work in this field. The best studies will be ones that combine 'omics techniques with ecology, physiology, or animal behavior, Davis' Whitehead says. "What 'omics does is it says, 'This gene is different between this species and that species, and this genetic program is differentially altered between this species and that species,'" he adds. "Where every other discipline comes in is in the question, 'Who cares?' There's a genetic difference, but does that actually affect anything important like a behavior or a physiology or a morphology? So really that link between genotype and phenotype is most important."

In addition, Glasgow's Buckley says, the combination of 'omics and more traditional scientific techniques will allow for more extensive studies of organisms in their natural environment. "It's going to be crucial that work on phenotypic variation … is combined with the potentially extensive genomic information you can get from these new techniques," he says. "It's still crucial to be studying systems that are responding in interesting ways and looking at them in the field, but these techniques perhaps allow for researchers to begin to explore the genetic variation in key traits that might be important for adapting to a changing environment, or genetic variation across populations and divergence within populations, and then relate that to how these populations differ in their ability to respond to different environments."

Importantly, he adds, studies should not only focus on the evolution of individual species in response to climate change, but how that response affects other organisms, and impacts on the possible formation of new ecosystems. "The interactions among organisms are critical in many cases. As organisms start to respond to climate change slightly differently, there will also be selection for species to keep pace with other organisms," he says. "If this doesn't happen, you have the possibility that plants lose important organisms that they interact with, and suffer the possibility of going extinct if they don't regain this interaction." Understanding evolutionary change in the broader ecosystem context — while not very well studied so far — is now a possible and "potentially exciting" area of research, Buckley says, thanks in part to this burgeoning field.

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