R2d2 Drives Selfish Sweeps in the House Mouse

Didion JP, Morgan AP, Yadgary L, Bell TA, Mcmullan RC, De Solorzano LO, Britton-Davidian J, Bult CJ, Campbell KJ, Castiglia R, Ching YH, Chunco AJ, Crowley JJ, Chesler EJ, Foerster DW, French JE, Gabriel SI, Gatti DM, Garland T, Giagia-Athanasopoulou EB, Gimenez MD, Grize SA, Gunduz I, Holmes A, Hauffe HC, Herman JS, Holt JM, Hua K, Jolley WJ, Lindholm AK, Lopez-Fuster MJ, Mitsainas G, Mathias MDL, Mcmillan L, Morgado Ramalhinho MDG, Rehermann B, Rosshart SP, Searle JB, Shiao MS, Solano E, Svenson KL, Thomas-Laemont P, Threadgill DW, Ventura J, Weinstock GM, Pomp D, Churchill GA, De Villena FPM (2016)

Publication Type: Journal article

Publication year: 2016

Journal

Book Volume: 33

Pages Range: 1381-1395

Journal Issue: 6

DOI: 10.1093/molbev/msw036

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.

Authors with CRIS profile

Involved external institutions

University of North Carolina at Chapel Hill United States (USA) (US) University of Montpellier / Université Montpellier France (FR) Howard Hughes Medical Institute United States (USA) (US) Università degli studi "La Sapienza" Italy (IT) Tzu Chi University / 慈濟大學 Taiwan (TW) Elon University United States (USA) (US) Leibniz-Institut für Zoo- und Wildtierforschung (IZW) Germany (DE) University of Lisbon / Universidade de Lisboa (ULisboa) Portugal (PT) National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK / NIDDKD) United States (USA) (US) Cornell University United States (USA) (US) Mahidol University / มหาวิทยาลัยมหิดล Thailand (TH) Texas A&M University United States (USA) (US) Autonomous University of Barcelona (UAB) / Universitat Autònoma de Barcelona Spain (ES) Jackson Laboratory for Genomic Medicine United States (USA) (US) National Institute of Environmental Health Sciences United States (USA) (US) University of California, Riverside (UCR) United States (USA) (US) University of Patras (UPATRAS) Greece (GR) Universidad Nacional de Misiones ( UNAM ) Argentina (AR) University of Zurich / Universität Zürich (UZH) Switzerland (CH) Ondokuz Mayıs University Turkey (TR) National Institute on Alcohol Abuse and Alcoholism (NIAAA) Germany (DE) Fondazione Edmund Mach di San Michele all'Adige Italy (IT) National Museums Scotland (NMS) / Taigh-tasgaidh Nàiseanta na h-Alba United Kingdom (GB) Universitat de Barcelona (UB) / University of Barcelona Spain (ES)

How to cite

APA:

Didion, J.P., Morgan, A.P., Yadgary, L., Bell, T.A., Mcmullan, R.C., De Solorzano, L.O.,... De Villena, F.P.-M. (2016). R2d2 Drives Selfish Sweeps in the House Mouse. Molecular Biology and Evolution, 33(6), 1381-1395. https://dx.doi.org/10.1093/molbev/msw036

MLA:

Didion, John P., et al. "R2d2 Drives Selfish Sweeps in the House Mouse." Molecular Biology and Evolution 33.6 (2016): 1381-1395.

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