The tiny, isolated gray wolf population on Isle Royale in Michigan has withered to two original members, but not because each animal carries a large number of harmful genes, according to a new analysis published in the May 29 issue of Science Advances.
Instead, each of the two remaining wolves from a population that has been followed for 60 years as part of the world's longest predator-prey study is exposed to a smaller pool of genes, making it more susceptible to inheriting two harmful copies of a particular gene, the researchers found.
When both parents contribute a copy of the same harmful gene to their offspring, recessive genes, which can encode physical deformities, are more likely to be expressed. The characteristically crooked spines of Isle Royale wolves are a recessive trait.
The paper's analysis of harmful gene variants in a population stands apart from a number of genomic studies in recent years that have mainly emphasized the accumulation of individual deleterious variations as a factor driving population decline. That idea has not been able to explain the plight of the inbred Isle Royale wolves — located in northwestern Lake Superior — because this wolf population declined sharply over just a few decades, with too little time for individual harmful genes to accumulate.
"It's important to understand that [the] total number [of deleterious mutations] does not necessarily tell you anything about the health of an individual or a population or a species," said Jacqueline A. Robinson, an evolutionary geneticist at the University of California, San Francisco and first author on the study.
In addition to illuminating the genetic underpinnings of this iconic wolf population's decline, she and her co-authors say the results of their work should shift researchers' thinking about conservation.
The findings from this study suggest that populations at risk for inbreeding should be bolstered through the introduction of individuals from historically small populations because these carry fewer potentially harmful gene copies, instead of adding animals from larger, more diverse gene pools which carry a greater number of individual harmful genes.
While this strategy may reduce the short-term risk of decline due to inbreeding, Robinson said it comes at the expense of future adaptability that could be fueled by a diverse gene pool — a tradeoff she believes must be evaluated on a situation-by-situation basis.
"With limited data sets and few empirical studies on which to draw, conservation has largely been guided by general rules of thumb, even though there is clearly no one-size-fits-all strategy to deal with the variety of factors threatening biodiversity," said Robinson.
While the Isle Royale wolf population once consisted of 50 wolves, today the original population has dwindled to a father and daughter pair that are also half siblings. The collapse of the Isle Royale wolf population occurred despite a reported genetic "rescue" in 1997 by a single migrant from the Minnesota mainland. Wolf genetic diversity on Isle Royale initially spiked after his arrival and inbreeding plummeted almost to zero, but the effect was short-lived.
"This male wolf was so much more virile than the resident wolves that every Isle Royale wolf was related to him within a few generations, and the initial benefits of the genetic rescue were quickly reversed as intense inbreeding set in amongst his descendants," said Robinson. "The dramatic turn of events on Isle Royale demonstrates the precarious existence of very small populations, where population dynamics can fluctuate over extremely short timescales."
To better characterize the genome-wide effects of intense inbreeding and isolation on this population, and their role in its decline, Robinson and colleagues analyzed mutations within the protein-coding regions of DNA from Isle Royale wolves and compared them with genetic data from wolves in nearby mainland Minnesota.
Strikingly, Isle Royale wolves did not exhibit a greater number of unique deleterious genes than the Minnesota group, but the proportion of wolves with paired harmful recessive gene copies in their genome was 38.4% higher in the Isle Royale population.
When the researchers compared Isle Royale genetic data with data collected from wolves around the world, they found distinct patterns in genomes corresponding with population size. Individuals from historically large populations more frequently contained two different gene copies at a gene location, while those from historically small populations more frequently contained short sequences of identical gene copy pairs. Those with a recent history of inbreeding — such as the Isle Royale wolves — had long regions of identical paired gene copies punctuating regions of gene copy mismatches.
They were surprised, however, to find that the Isle Royale wolves did not have the lowest genetic diversity in the dataset, suggesting that there may be a more complicated relationship between genetic diversity and genetic health than previously thought.
Today, a more robust genetic rescue effort is underway. Between autumn 2018 and spring 2019, new wolves were introduced to Isle Royale from nearby mainland Ontario and Michipicoten Island in northeastern Lake Superior, bringing the island's total to 15. To delay inbreeding, most of the wolves were not closely related, but to Robinson's knowledge the historical population size was not considered in choosing which wolves to bring to the island. The relationship between genetics and population size could be considered in future efforts to conserve at-risk populations based on the results of this study.
Conservationists hope the newcomers will help revitalize Isle Royale's wolves, which balance the ecosystem by hunting moose that could otherwise deplete native vegetation.