Science + Technology

Biologists solve mystery of black wolves

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Why do nearly half of North American wolves have black coats while European wolves are overwhelmingly gray or white? The surprising answer, according to teams of biologists and molecular geneticists from Stanford University, UCLA, Sweden, Canada and Italy, is that the black coats are the result of historical matings between black dogs and wild gray wolves.
 
The research, federally funded by the National Science Foundation, appears Feb. 5 in the online edition of the journal Science and will be published later in the journal's print edition.
 
The scientists used molecular genetic techniques to analyze DNA sequences from 150 wolves, about half of them black, in Yellowstone National Park, which covers parts of Wyoming, Montana and Idaho. They found that a novel mutated variant of a gene in dogs, known as the K locus, is responsible for black coat color and was transferred to wolves through mating.
 
The biologists are unsure of when the black coat color was transferred from dogs to wolves, but they believe it was not a recent occurrence; the black coat could not have spread as widely as it has throughout North America in just a few hundred years, they say. They suspect the transfer took place sometime before the arrival of Europeans to North America and involved dogs that were here with Native Americans.
 
"This is the first example where a gene mutation originated in a domesticated species, was transferred to and became very common in a closely related wild species," said Robert Wayne, a UCLA professor of ecology and evolutionary biology and co-author of the Science paper.
 
"Although genes that evolve under domestication may be transferred to wild species, they generally do not proliferate in the wild because the natural context is so different from that under domestication," Wayne said. "No one would have guessed that the common black coat color in North American wolves came from dogs — there is no precedent for it. Moreover, for whatever reason, the transfer of the black coat-color gene from dogs to wolves and its success in the wild occurred uniquely in North America.
 
"Most mutations we see in dogs have been selected by humans, and we intuitively think they are unique to dogs," he said. "We don't think of short-legged wolves like dachshunds or wild wolves that look like Dalmatians. The surprise of this study is that black wolves have their black coat coloration as a gift from dogs. The products of artificial selection had added substantially to the genetic legacy of a wild species."
 
Scientists have thought that coat color is related to camouflage, perhaps to hide wolves from their prey or from one another.
 
"Apparently, natural selection has increased the frequency of black coat color dramatically in wolf populations across North America," Wayne said. "It must have adaptive value that we don't yet understand. It could be camouflage, or strengthening the immune system to combat pathogens, or it could reflect a preference to mate with individuals of a different coat color."
 
Does this research have implications beyond dogs and wolves?
 
"The underlying assumption is that genes from one species will be contained and not enter another species on a massive scale; this may not be true," Wayne said. "There may be implications for genetically modified organisms."
 
"This work shows how domestication can preserve and ultimately enrich the genetic legacy of the original natural populations," said Gregory Barsh, a professor of genetics at Stanford University's School of Medicine and co-author of the Science paper. "Our work is on wolves, but there are many other examples of domestic plants — wheat, rice, maize, soybean — and animals — bison, cattle, cats — where gene flow from domesticated to natural populations has been documented."
 
The lead authors of the paper are Tovi Anderson, a graduate student in Barsh's Stanford laboratory, and Bridgett vonHoldt, a UCLA graduate student of ecology and evolutionary biology who works in Wayne's laboratory.
 
As part of the research on the Yellowstone wolves, VonHoldt conducted a genome scan and studied more than 50,000 genetic markers in order to assess genetic variation across wolf populations in relation to dogs. She and her colleagues examined whether there was any evidence elsewhere in the genome indicating that black wolves recently hybridized with dogs but could not find any.
 
Black coyotes also have the same coat-color gene as domestic dogs, Anderson, vonHoldt and the co-authors report.
 
The research was conducted by laboratory and field scientists with diverse backgrounds in conservation biology, ecology and molecular genetics.
 
The collaboration will help to refine concepts relevant to both genetics and conservation biology with respect to understanding how different traits arise during evolution and how biological diversity can be nurtured and maintained, the scientists said.
 
"My main interest is to describe the genetics of dog domestication — the geographic location of domestication and the genetic changes that led to the distinctive body forms evident in so many breeds," vonHoldt said. "I'm able to use a genome approach and look at many points along the dog genome to find interesting regions and whether these regions contain genes with known functions, and to extrapolate what that means for the domestication process of dogs.
 
"We're trying to figure out whether the black coat color provides a fitness or behavioral advantage," she added, noting that Yellowstone National Park has a wealth of observational data that "we can integrate with our genetic data."
 
"We can scan the dog's genome and find associations between a particular marker and a trait like foreshortened limbs or a specific coat color, or even behavioral traits," Wayne said. "We then examine the genes near those markers and identify candidates that may be responsible for the specific trait. Our hope is that we will find the genetic basis for traits having to do with behavior, speed, longevity or fecundity — all these traits that we measure in wild populations, but we do not yet understand their genetic basis."
 
Yellowstone is home to the wolf population about which the most is known, Wayne said. Their behavior and reproduction have been well studied, including by one of Wayne's graduate students, Daniel Stahler, a co-author of the Science paper who works as a biologist for the Yellowstone National Park Gray Wolf Restoration Project.
 
"The wolves of Yellowstone represent an unparalleled population for studying the inheritance of traits," Wayne said. "In Yellowstone, we have followed very precisely the inheritance of coat color throughout the entire wolf population and document that coat color is a trait inherited with just one gene involved, with two forms — one causing white and one causing black. This is the most comprehensive genealogical analysis of a North American carnivore population ever undertaken."
 
Other co-authors on the paper are Sophie Candille, from Barsh's Stanford laboratory; Marco Musiani, a professor at the University of Calgary and former postdoctoral scholar in Wayne's laboratory; Claudia Greco, a graduate student from Italy who previously worked in Wayne's laboratory, and her adviser, Ettore Randi; Douglas W. Smith, project leader for the Yellowstone National Park Gray Wolf Restoration Project; Badri Padhukasahasram, a graduate student in the department of biological statistics and computational biology at Cornell University; Jennifer Leonard of Sweden's Uppsala University, a former Ph.D. student in Wayne's laboratory; Carlos Bustamante, a statistical population geneticist in the department of biological statistics and computational biology at Cornell; Elaine Ostrander of the National Human Genome Research Institute; and Hua Tang, from Barsh's laboratory.
 
In previous research, Wayne and colleagues used molecular genetic techniques to determine that dogs have ancient origins, and that the first Americans to arrive in the New World more than 12,000 years ago brought domesticated dogs with them. They have also found that dogs have been living in close association with humans much longer than any other domestic animal, have confirmed that dogs evolved from wolves, and have confirmed that today's domestic horse resulted from the interbreeding of many lines of wild horses in multiple locations and was not confined to a small area or a single culture.
 
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