Genetic rescue of endangered species may risk bad mutations slipping through
Study hints there are ecological secrets behind relocation success
COLUMBUS, Ohio – The established conservation practice of relocating animals from large, genetically diverse populations to small communities of inbred endangered species may risk introducing more damaging than beneficial gene variants into the threatened group, a new study suggests.
Analysis of genomes of Eastern massasauga rattlesnakes showed that, by the numbers, more deleterious than adaptation-enabling mutations were present in the more genetically diverse donor animals selected in a hypothetical scenario to join a small, isolated population.
Because donor relocation, known as assisted gene flow, has a good track record of stabilizing recipient populations, the researchers say this finding suggests there must be more at play in rescue efforts than purely genetics that help species survive – namely, environmental characteristics that support long-term persistence.
“We have a little bit of a paradox here. The genetic analysis says genetic rescue is maybe not good, or at best, it’s a wash,” said H. Lisle Gibbs, professor of evolution, ecology and organismal biology at The Ohio State University and senior author of the study.
“But when you look at other studies of assisted gene flow activity for other rare organisms, the small population usually grows. Genetics suggests even though rescue works by increasing the numbers of individuals in the first few generations by reducing inbreeding effects, it could be risky long-term. And so, we should look more closely at other factors, especially ecological factors, that may allow the species breathing room for the evolutionary factors to work.”
Samarth Mathur, a former postdoctoral research scientist in Gibbs’ lab, was the first author of the study. The research was published recently in the journal Molecular Ecology.
Decades of previous research has linked the lack of genetic diversity and related limitation on adaptation in endangered species to population decline and extinction in plants, insects, birds and mammals.
In a 2023 study identifying about 150 species considered good candidates for assisted gene flow, the authors cited numerous studies showing the effectiveness of relocating genetically diverse species and urged wider adoption of the strategy.
“Taking a small number of individuals from a larger population and moving them to a smaller population is traditionally justified by the idea that because of low numbers, a small population has lost a lot of the good copies of many genes that led to adaptation,” Gibbs said. “Further, the idea is that you can replenish this with individuals from a larger population, which is more genetically diverse, and they bring the good copies of those genes with them.
“The point of this paper is to show our ability to identify these categories of good and bad copies for every gene, and to actually ask, are these hypothetical donors genetically good enough for long-term success?”
In other words, Gibbs and Mathur are the first to put the genetics of the practice to the test on a gene-by-gene basis.
“When you move individuals from a big population to a small population, you bring both kinds of variation – not just the good kind alone. There is bad stuff that’s also part of the package,” Gibbs said. “This is the first time anyone has put this together and asked how important the good variation is, and how to measure it against the burden of bad variation that it also brings.”
The analysis involved whole genome sequences from 152 Eastern massasauga rattlesnakes being studied in 14 sites in the United States and Canada. Zeroing in on circumstances for this species in Ohio, researchers compared possible scenarios involving two donor populations and three recipient populations to identify the best donor-recipient fit for assisted gene flow.
The analysis involved studying single-nucleotide polymorphisms (or SNPs, pronounced “snips”) in genes that carry instructions for functional proteins. Each gene contains two copies (called alleles) which could be functionally different in some cases because it carries a mutation, or SNP. These mutations can change the function or the expression of that gene, and this study compared these differences by measuring the numbers of deleterious and adaptive mutations carried by different populations.
Overall, the analysis showed minimal differences between the two donor populations’ suitability for relocation but suggested all donor groups would have substantial effects on functional genetic variation in recipient populations.
In one example scenario, donor snakes would contribute to a recipient population a 34% increase in positive variants, a 36% increase in moderately damaging mutations, and a 32% increase in the most severe loss-of-function mutations that knock out a gene.
“The numbers suggest you get a little bump in terms of good mutations and a little bump in terms of masking bad mutations which reduce inbreeding effects, but then you get a whole bunch of bad mutations, too. We’re estimating good and bad mutations using a purely computational approach to quantify the net effect, which is to introduce lots of small-effect bad mutations,” Gibbs said.
There is another school of thought when it comes to assisted gene flow – that a species’ ability to adapt to its local environment is the whole ballgame and, therefore, outsiders’ genes could disrupt that adaptability.
In this study, only 7% of the identified adaptive mutations in donor snakes were connected to their adaptation to another region of Ohio.
“So, there are a few, but not very many maladapted genes, which suggests concern about local adaptation is probably not a major risk,” Gibbs said. “So maybe the ecological effects of rescue are overwhelmingly positive, and the increase in numbers may compensate for any risk of long-term negative genetic effects.”
The statistical techniques Mathur and Gibbs developed for this study could be used for any proposed assisted gene flow strategy for which genome sequences are available.
“This isn’t just about snakes. It’s about big populations and small populations, and so we think the result is general,” Gibbs said. “Our key contribution is actually measuring the risk involved with genetic rescue in a real-world situation. It will be of interest to use our statistical techniques to see if the risk of potential increase in mutation load for Eastern massasaugas holds for other endangered species.”
This work was supported by the State Wildlife Grants Program, administered jointly by the U.S. Fish and Wildlife Service and the Ohio Division of Wildlife, and the Ohio Biodiversity Conservation Partnership, with which Gibbs and Mathur are affiliated.
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Contact: H. Lisle Gibbs, Gibbs.128@osu.edu
Written by Emily Caldwell, Caldwell.151@osu.edu; 614-292-8152
Journal
Molecular Ecology
Article Title
Genomic Evaluation of Assisted Gene Flow Options in an Endangered Rattlesnake
