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The crucial role of genome-wide genetic variation in conservation

Marty Kardos, Ellie Armstrong, Sarah Fitzpatrick, Samantha Hauser, Phil Hedrick, Josh Miller, David A. Tallmon, W. Chris Funk
doi: https://doi.org/10.1101/2021.07.05.451163
Marty Kardos
1Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA
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  • For correspondence: martin.kardos@noaa.gov
Ellie Armstrong
2Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
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Sarah Fitzpatrick
3W.K. Kellogg Biological Station; Department of Integrative Biology; Ecology, Evolution, and Behavior Program, Michigan State University, 3700 Gull Lake Drive, Hickory Corners, MI 49060, USA
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Samantha Hauser
4Department of Biological Sciences, University of Wisconsin – Milwaukee, P.O. Box 413, Milwaukee, WI 53211, USA
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Phil Hedrick
5School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA
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Josh Miller
6San Diego Zoo Wildlife Alliance, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA
7Polar Bears International, PO Box 3008, Bozeman, MT, USA
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David A. Tallmon
8Biology and Marine Biology Program, University of Alaska Southeast, 11066 Auke Lake Way Juneau, AK 99801, USA
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W. Chris Funk
9Department of Biology, Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO 80523, USA
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Abstract

The unprecedented rate of extinction calls for efficient use of genetics to help conserve biodiversity. Several recent genomic and simulation-based studies have argued that the field of conservation biology has placed too much focus on the conservation of genome-wide genetic variation, and that this approach should be replaced with another that focuses instead on managing the subset of functional genetic variation that is thought to affect fitness. Here, we critically evaluate the feasibility and likely benefits of this approach in conservation. We find that population genetics theory and empirical results show that the conserving genome-wide genetic variation is generally the best approach to prevent inbreeding depression and loss of adaptive potential from driving populations towards extinction. Focusing conservation efforts on presumably functional genetic variation will only be feasible occasionally, often misleading, and counterproductive when prioritized over genome-wide genetic variation. Given the increasing rate of habitat loss and other environmental changes, failure to recognize the detrimental effects of lost genome-wide variation on long-term population viability will only worsen the biodiversity crisis.

Competing Interest Statement

The authors have declared no competing interest.

  • Glossary

    Adaptive potential
    The ability of a population to evolve adaptively in response to selection. Usually measured as narrow sense heritability (the proportion of phenotypic variance attributed to additive genetic effects).
    Drift load
    The reduction in mean fitness of a population due to homozygosity for deleterious alleles.
    F
    The individual inbreeding coefficient: the identical-by-descent fraction of an individual’s genome.
    Genetic load
    The reduction in fitness due to all genetic effects arising from both segregating and fixed deleterious alleles.
    Genetic rescue
    Increase in population growth or reduction in genetic load arising from the immigration of individuals with new alleles.
    h
    the dominance coefficient. A derived allele is recessive when h=0 (heterozygous genotypes have the same mean fitness as homozygous wildtypes), and dominant when h=1 (heterozygous genotypes have the same mean fitness as homozygous derived allele genotype), and additive when h=0.5 (heterozygous genotypes have fitness midway between the alternative homozygous genotypes).
    H
    heterozygous fraction of an individual’s genome.
    Hard selection
    Where an individual’s absolute fitness depends only on its phenotype or genotype and is independent of the phenotypes or genotypes of other individuals in the population.
    Identical-by-descent
    two segments of DNA are identical-by-descent when they both descend from a single haploid genome in recent ancestor.
    Inbreeding
    mating between relatives.
    Inbreeding depression
    reduced fitness of individuals whose parents are related.
    Inbreeding load
    A measure of the potential for inbreeding to reduce fitness, measured by the number of Lethal equivalents, which is a set of alleles that would on average cause one death when homozygous.
    π
    nucleotide diversity: expected proportion of nucleotide differences between randomly chosen pairs of haploid genomes in a population.
    Purging
    Reduction in the inbreeding load owing to deleterious partially recessive alleles being exposed to purifying selection via inbreeding.
    Soft selection
    Selection where an individual’s fitness depends on its phenotype or genotype relative to others in the same population.
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    Posted July 06, 2021.
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    The crucial role of genome-wide genetic variation in conservation
    Marty Kardos, Ellie Armstrong, Sarah Fitzpatrick, Samantha Hauser, Phil Hedrick, Josh Miller, David A. Tallmon, W. Chris Funk
    bioRxiv 2021.07.05.451163; doi: https://doi.org/10.1101/2021.07.05.451163
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    The crucial role of genome-wide genetic variation in conservation
    Marty Kardos, Ellie Armstrong, Sarah Fitzpatrick, Samantha Hauser, Phil Hedrick, Josh Miller, David A. Tallmon, W. Chris Funk
    bioRxiv 2021.07.05.451163; doi: https://doi.org/10.1101/2021.07.05.451163

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