R2d2 Drives Selfish Sweeps in the House Mouse

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  • Didion, John P.
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • Morgan, Andrew P.
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • Yadgary, Liran
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • Bell, Timothy A.
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • McMullan, Rachel C.
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • De Solorzano, Lydia Ortiz
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
  • Britton-Davidian, Janice
    • Other Affiliation: Institut des Sciences de l'Evolution; Université de Montpellier; CNRS; IRD; EPHE
  • Bult, Carol J.
    • Other Affiliation: Jackson Laboratory
  • Campbell, Karl J.
    • Other Affiliation: School of Geography; Planning and Environmental Management; University of Queensland
  • Castiglia, Riccardo
    • Other Affiliation: Department of Biology and Biotechnologies Charles Darwin; University of Rome la Sapienza
  • Ching, Yung-Hao
    • Other Affiliation: Department of Molecular Biology and Human Genetics; Tzu Chi University
  • Chunco, Amanda J.
    • Other Affiliation: Department of Environmental Studies; Elon University
  • Crowley, James J.
    • Affiliation: School of Medicine, Department of Genetics
  • Chesler, Elissa J.
    • Other Affiliation: Jackson Laboratory
  • Förster, Daniel W.
    • Other Affiliation: Department of Evolutionary Genetics; Leibniz-Institute for Zoo and Wildlife Research
  • French, John E.
    • Other Affiliation: National Toxicology Program; National Institute of Environmental Sciences; NIH
  • Gabriel, Sofia I.
    • Other Affiliation: Department of Animal Biology and CESAM; Centre for Environmental and Marine Studies; Faculty of Sciences; University of Lisbon
  • Gatti, Daniel M.
    • Other Affiliation: Jackson Laboratory
  • Garland, Theodore
    • Other Affiliation: Department of Biology; University of California Riverside
  • Giagia-Athanasopoulou, Eva B.
    • Other Affiliation: Section of Animal Biology; Department of Biology; University of Patras
  • Giménez, Mabel D.
    • Other Affiliation: Instituto de Biología Subtropical; CONICET - Universidad Nacional de Misiones
  • Grize, Sofia A.
    • Other Affiliation: Institute of Evolutionary Biology and Environmental Studies; University of Zurich
  • Gündüz, Islam
    • Other Affiliation: Department of Biology; Faculty of Arts and Sciences; University of Ondokuz Mayis
  • Holmes, Andrew
    • Other Affiliation: Laboratory of Behavioral and Genomic Neuroscience; National Institute on Alcohol Abuse and Alcoholism; NIH
  • Hauffe, Heidi C.
    • Other Affiliation: Department of Biodiversity and Molecular Ecology; Research and Innovation Centre; Fondazione Edmund Mach
  • Herman, Jeremy S.
    • Other Affiliation: Department of Natural Sciences; National Museums Scotland
  • Holt, James M.
    • Affiliation: College of Arts and Sciences, Department of Computer Science
  • Hua, Kunjie
    • Affiliation: School of Medicine, Department of Genetics
  • Jolley, Wesley J.
    • Other Affiliation: Island Conservation
  • Lindholm, Anna K.
    • Other Affiliation: Institute of Evolutionary Biology and Environmental Studies; University of Zurich
  • López-Fuster, María J.
    • Other Affiliation: Faculty of Biology; Universitat de Barcelona
  • Mitsainas, George
    • Other Affiliation: Section of Animal Biology; Department of Biology; University of Patras
  • Da Luz Mathias, Maria
    • Other Affiliation: Department of Animal Biology and CESAM; Centre for Environmental and Marine Studies; Faculty of Sciences; University of Lisbon
  • McMillan, Leonard
    • Affiliation: College of Arts and Sciences, Department of Computer Science
  • Ramalhinho, Maria Da Graça Morgado
    • Other Affiliation: Department of Animal Biology and CESAM; Centre for Environmental and Marine Studies; Faculty of Sciences; University of Lisbon
  • Rehermann, Barbara
    • Other Affiliation: Immunology Section; Liver Diseases Branch; National Institute of Diabetes and Digestive and Kidney Diseases; NIH
  • Rosshart, Stephan P.
    • Other Affiliation: Immunology Section; Liver Diseases Branch; National Institute of Diabetes and Digestive and Kidney Diseases; NIH
  • Searle, Jeremy B.
    • Other Affiliation: Department of Ecology and Evolutionary Biology; Cornell University
  • Shiao, Meng-Shin
    • Other Affiliation: Research Center; Faculty of Medicine; Ramathibodi Hospital; Mahidol University
  • Solano, Emanuela
    • Other Affiliation: Department of Biology and Biotechnologies Charles Darwin; University of Rome la Sapienza
  • Svenson, Karen L.
    • Other Affiliation: Jackson Laboratory
  • Thomas-Laemont, Patricia
    • Other Affiliation: Department of Environmental Studies; Elon University
  • Threadgill, David W.
    • Other Affiliation: Department of Molecular and Cellular Medicine; Texas AandM University
  • Ventura, Jacint
    • Other Affiliation: Departament de Biologia Animal; de Biologia Vegetal y de Ecologia; Facultat de Biociències; Universitat Autònoma de Barcelona
  • Weinstock, George M.
    • Other Affiliation: Jackson Laboratory for Genomic Medicine
  • Pomp, Daniel
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: Carolina Center for Genome Sciences
  • Churchill, Gary A.
    • Other Affiliation: Jackson Laboratory
  • De Villena, Fernando Pardo-Manuel
    • Affiliation: School of Medicine, Department of Genetics
    • Other Affiliation: University of North Carolina at Chapel Hill
Abstract
  • A selective sweep is the result of strong positive selection driving newly occurring or standing genetic variants to fixation, and can dramatically alter the pattern and distribution of allelic diversity in a population. Population-level sequencing data have enabled discoveries of selective sweeps associated with genes involved in recent adaptations in many species. In contrast, much debate but little evidence addresses whether “selfish” genes are capable of fixation—thereby leaving signatures identical to classical selective sweeps—despite being neutral or deleterious to organismal fitness. We previously described R2d2, a large copy-number variant that causes nonrandom segregation of mouse Chromosome 2 in females due to meiotic drive. Here we show population-genetic data consistent with a selfish sweep driven by alleles of R2d2 with high copy number (R2d2HC) in natural populations. We replicate this finding in multiple closed breeding populations from six outbred backgrounds segregating for R2d2 alleles. We find that R2d2HC rapidly increases in frequency, and in most cases becomes fixed in significantly fewer generations than can be explained by genetic drift. R2d2HC is also associated with significantly reduced litter sizes in heterozygous mothers, making it a true selfish allele. Our data provide direct evidence of populations actively undergoing selfish sweeps, and demonstrate that meiotic drive can rapidly alter the genomic landscape in favor of mutations with neutral or even negative effects on overall Darwinian fitness. Further study will reveal the incidence of selfish sweeps, and will elucidate the relative contributions of selfish genes, adaptation and genetic drift to evolution.
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  • Article
Rights statement
  • In Copyright
Journal title
  • Molecular Biology and Evolution
Journal volume
  • 33
Journal issue
  • 6
Language
  • English
ISSN
  • 1537-1719
  • 0737-4038

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