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Mol Biol Evol. 2016 Jun;33(6):1381-95. doi: 10.1093/molbev/msw036. Epub 2016 Feb 15.

R2d2 Drives Selfish Sweeps in the House Mouse.

Author information

1
Department of Genetics, The University of North Carolina at Chapel Hill Lineberger Comprehensive Cancer Center, The University of North Carolina at Chapel Hill Carolina Center for Genome Science, The University of North Carolina at Chapel Hill fernando@med.unc.edu.
2
Department of Genetics, The University of North Carolina at Chapel Hill Lineberger Comprehensive Cancer Center, The University of North Carolina at Chapel Hill Carolina Center for Genome Science, The University of North Carolina at Chapel Hill.
3
Institut des Sciences de l'Evolution, Université De Montpellier, CNRS, IRD, EPHE, Montpellier, France.
4
The Jackson Laboratory, Bar Harbor, ME.
5
Island Conservation, Puerto Ayora, Galápagos Island, Ecuador School of Geography, Planning & Environmental Management, The University of Queensland, St Lucia, QLD, Australia.
6
Department of Biology and Biotechnologies "Charles Darwin", University of Rome "La Sapienza", Rome, Italy.
7
Department of Molecular Biology and Human Genetics, Tzu Chi University, Hualien City, Taiwan.
8
Department of Environmental Studies, Elon University.
9
Department of Genetics, The University of North Carolina at Chapel Hill.
10
Department of Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research, Berlin, Germany.
11
National Toxicology Program, National Institute of Environmental Sciences, NIH, Research Triangle Park, NC.
12
Department of Animal Biology & CESAM - Centre for Environmental and Marine Studies, Faculty of Sciences, University of Lisbon, Lisboa, Portugal.
13
Department of Biology, University of California Riverside.
14
Section of Animal Biology, Department of Biology, University of Patras, Patras, Greece.
15
Instituto de Biología Subtropical, CONICET - Universidad Nacional de Misiones, Posadas, Misiones, Argentina.
16
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
17
Department of Biology, Faculty of Arts and Sciences, University of Ondokuz Mayis, Samsun, Turkey.
18
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD.
19
Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'adige, TN, Italy.
20
Department of Natural Sciences, National Museums Scotland, Edinburgh, United Kingdom.
21
Department of Computer Science, The University of North Carolina at Chapel Hill.
22
Island Conservation, Santa Cruz, CA.
23
Faculty of Biology, Universitat de Barcelona, Barcelona, Spain.
24
Immunology Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD.
25
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY.
26
Research Center, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.
27
Department of Veterinary Pathobiology, Texas A&M University, College Station Department of Molecular and Cellular Medicine, Texas A&M University, College Station.
28
Departament de Biologia Animal, de Biologia Vegetal y de Ecologia, Facultat de Biociències, Universitat Autònoma de Barcelona, Barcelona, Spain.
29
Jackson Laboratory for Genomic Medicine, Farmington, CT.
30
Department of Genetics, The University of North Carolina at Chapel Hill Carolina Center for Genome Science, The 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 (R2d2(HC)) in natural populations. We replicate this finding in multiple closed breeding populations from six outbred backgrounds segregating for R2d2 alleles. We find that R2d2(HC) rapidly increases in frequency, and in most cases becomes fixed in significantly fewer generations than can be explained by genetic drift. R2d2(HC) 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.

KEYWORDS:

House Mouse.; Meiotic Drive; R2d2; Selective Sweep; Selfish Genes

PMID:
26882987
PMCID:
PMC4868115
DOI:
10.1093/molbev/msw036
[Indexed for MEDLINE]
Free PMC Article

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