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Why Are There So Many Black Wolves In Yellowstone?

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Black wolves are either absent or very rare in most parts of their range, but are mysteriously common in some parts of North America

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Black wolves are among the most iconic animals at Yellowstone National Park. People travel from around the world to Yellowstone to catch a glimpse of its famous black wolves.

Historically, most wolves are grey — or white in the far north — whereas black is not a natural color amongst wolves. But Yellowstone is truly exceptional in this regard: almost half of its wolves are black.

Many factors affect pelage color: local weather conditions, elevation, latitude, local parasites, food, and predators. Further, spatial variations can create a measurable gradient in a single trait, like coat color, across a species’ geographical range, usually along a line of environmental or geographic transition. This transition line is known as a cline.

In North America, the proportion of black to grey wolves increases along a southward cline that stretches from Arctic Canada along the Rocky Mountains in the United States down towards Mexico (Figure 1A). Why?

An international team of scientists investigated this long-standing mystery.

“In most parts of the world black wolves are absent or very rare, yet in North America they are common in some areas and absent in others”, said the study’s senior author, Tim Coulson, a Professor of Biology at the University of Oxford. Professor Coulson’s research focuses on ecological and evolutionary impacts of environmental change on natural systems, and how different species and ecosystems respond to different types of environmental change.

“Scientists have long wondered why”, Professor Coulson said in a statement. “We now have an explanation based on wolf surveys across North America, and modeling motivated by extraordinary data collected by co-authors who work in Yellowstone.”

This fascinating study indicates that coat color reflects an individual wolf’s immunity to the canine distemper virus (CDV), and further, observed changes in the proportion of black wolves in a population may be linked to the frequency of CDV disease outbreaks, combined with changes in the wolves’ mating behavior, particularly whether they select a mate with the same or a different coat color to their own.

The genetics of black pelage in wolves

Coat color in wolves, Canis lupus, is determined by one of two gene variants, or alleles. One allele, the ancestral k allele, creates the normal Agouti coat color seen in grey wolves. However, a three-nucleotide deletion in the K locus gene results in a protein that prevents Agouti function, thereby creating the dominant inheritance of a black coat. Previous work proposes that the black coat color allele was introduced into the North American wolf population just once, around 7,250 years ago, by dogs carrying the gene that accompanied people who migrated across the Bering Strait. Since then, this allele has undergone one of the most rapid spreads known for an adaptive gene variant amongst vertebrates (ref).

Both homozygous KK and the heterozygous Kk individuals have black coats that are visually indistinguishable, but these two genotypes have very different fitness consequences (ref).

“Black homozygotes are very uncommon,” explained lead author of the study, evolutionary ecologist Sarah Cubaynes, in email. “They represent less than 5% of the population in Yellowstone.” Professor Cubaynes is a Lecturer at the University of Montpellier, where she uses biostatistics to understand evolutionary and ecological changes in populations.

Are black homozygotes infertile?

“We had very few black homozygote females that reproduced in our data, so it was not possible to estimate their fertility,” Professor Cubaynes told me in email.

Do black homozygotes even survive to adulthood?

“We had a few black homozygotes in our survival data, so we estimated a much lower survival rate than for grey or black heterozygotes — with lower precision, but still their mean survival was clearly lower”, Professor Cubaynes elaborated in email. “This is also because they have low vital rates that they are so uncommon in populations — it could be that they die very young before reaching adulthood.”

The origin of Canine Distemper Virus

Clearly, coat color itself is not what is under selection, but rather, the dominant black K allele has another, less obvious, function that confers a strong selective advantage in certain environments (ref). The protein encoded by the K allele is a ß-defensin protein that not only is involved in creating black coat color but it also plays a direct role in immune function. This protein is part of the molecular pathway that mediates the immune response to respiratory infections, particularly those caused by CDV, a viral pathogen of carnivores that can cause substantial mortality among immunologically naïve individuals, particularly juveniles.

The origin of CDV itself is still debated. It appears to be a very young virus that first emerged in North America in the 1730s, after evolving from the cattle virus, rinderpest, which accompanied European settlers and their livestock. However, a more recent hypothesis proposes that CDV emerged in the 1500s after Spanish conquistadores carrying a measles virus invaded South America, along with their dogs.

The delicate balance between surviving CDV and having a big family

Black heterozygotes (Kk) show a more robust immune response to CDV, but at the cost of producing fewer pups per litter. In contrast, female grey (kk) wolves, which lack this innate immune boost, produced litters that were 25% larger than those of black females.

Professor Cubaynes and her collaborators tested the prediction that coat color varies with CDV occurrence. They analyzed 12 wolf populations and found that wolves with CDV antibodies are indeed more likely to be black, especially older wolves — probably because they are more likely to have survived the infection and were alive to later be sampled by scientists (Figure 1B). Based on these data, Professor Cubaynes and her collaborators created a predictive model to assess whether CDV outbreaks affected the probability of a wolf being black. This model revealed a positive correlation between population-level CDV disease exposure and whether an individual is black or grey (Figure 1C).

Professor Cubaynes and her collaborators then wanted to better pin down the relationship between CDV and coat color. They examined the wolves of Yellowstone National Park, where the population is split almost evenly between black and grey wolves, and where CDV outbreaks occur approximately every five years. The scientists analyzed more than 20 years of data collected from the Yellowstone wolves and found that black wolves were more likely to survive CDV outbreaks than grey wolves.

But how are both coat colors maintained in the population? Professor Cubaynes and her collaborators hypothesized that the Yellowstone wolves were actually choosing mates whose coat color was different from their own to maximize the chance their pups would have black coats.

“Using a predictive model based on empirical Yellowstone wolf data, we were able to determine that fitness is greatest when wolves mate ‘disassortatively’ [mating between a black and a gray wolf] in the presence of disease outbreaks at least once every five years,” said Ellen Brandell, one of the study’s co-authors who works as a wildlife research scientist at Colorado Parks and Wildlife.

Indeed, this mate choice behavior is what precisely what is observed in the Yellowstone wolf population.

“This corresponds with wolf behavior and disease in Yellowstone, where black-gray pairs are observed more than expected and five canine distemper outbreaks have occurred in 24 years,” Dr Brandell explained in a statement.

The team’s model predicted that black wolves do better when CDV outbreaks are common, whilst grey wolves do better when CDV outbreaks are rare.

“Additionally, under this scenario, the model accurately predicts the observed coat color frequency in Yellowstone wolves,” Dr Brandell said. “Together, these results explain the geographic patterns of the coloration of an apex predator.”

In addition to the overall accuracy of this model, what was the most interesting or rewarding aspect of this study?

“What I love about this study is how we have been able to bring together experts from so many fields and a range of approaches to show how disease can have remarkable impacts of wolf coat color and behavior,” said Peter Hudson, Willaman Professor of Biology at Pennsylvania State University, where his research focuses on the ecology of wildlife diseases.

It’s interesting to note that many animals, including insects, amphibians, birds and mammals, show associations between observable color and disease resistance. In such situations, either the presence a particular disease or how frequently a disease outbreak occurs may play an important role in the color of an animal’s chosen mate.

“We are learning that disease is a major evolutionary driver that impacts so many aspects of animal populations.”

Source:

Sarah Cubaynes, Ellen E. Brandell, Daniel R. Stahler, Douglas W. Smith, Emily S. Almberg, Susanne Schindler, Robert K. Wayne, Andrew P. Dobson, Bridgett M. vonHoldt, Daniel R. MacNulty, Paul C. Cross, Peter J. Hudson, Tim Coulson (2022). Disease outbreaks select for mate choice and coat color in wolves, Science | doi:10.1126/science.abi8745


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