R2d2 drives selfish sweeps in the house mouse

Autores
Didion, John P.; Morgan, Andrew P.; Yadgary, Liran; Bell, Timothy A.; McMullan, Rachel C.; Ortiz de Solorzano, Lydia; Britton-Davidian, Janice; Bult, Carol J.; Campbell, Karl J.; Castiglia, Riccardo; Ching, Yung-Hao; Chunco, Amanda J.; Crowley, James J.; Chesler, Elissa J.; Förster, Daniel W.; French, John E.; Gabriel, Sofia I.; Gatti, Daniel M.; Garland, Theodore Jr; Giagia Athanasopoulou, Eva B.; Giménez, Mabel Dionisia; Grize, Sofia A.; Gündüz, Islam; Holmes, Andrew; Hauffe, Heidi C.; Herman, Jeremy S.; Holt, James M.; Kunjie, Hua; Jolley, Wesley J.; Pardo Manuel de Villena, Fernando
Año de publicación
2016
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Didion, John P.. University of North Carolina; Estados Unidos
Fil: Morgan, Andrew P.. University of North Carolina; Estados Unidos
Fil: Yadgary, Liran. University of North Carolina; Estados Unidos
Fil: Bell, Timothy A.. University of North Carolina; Estados Unidos
Fil: McMullan, Rachel C.. University of North Carolina; Estados Unidos
Fil: Ortiz de Solorzano, Lydia. University of North Carolina; Estados Unidos
Fil: Britton-Davidian, Janice. Université de Montpellier. Instituto Des Sciences de L'evolution; Francia
Fil: Bult, Carol J.. The Jackson Laboratory; Estados Unidos
Fil: Campbell, Karl J.. The University Of Queensland; Australia
Fil: Castiglia, Riccardo. Universita Di Roma; Italia
Fil: Ching, Yung-Hao. University Tzu Chi. Department of Molecular Biology and Human Genetics; China
Fil: Chunco, Amanda J.. University of North Carolina; Estados Unidos
Fil: Crowley, James J.. University of North Carolina; Estados Unidos
Fil: Chesler, Elissa J.. The Jackson Laboratory; Estados Unidos
Fil: Förster, Daniel W.. Leibniz - Institute for Zoo and Wildlife Research; Alemania
Fil: French, John E.. National Institute of Environmental Sciences; Estados Unidos
Fil: Gabriel, Sofia I.. Universidade de Lisboa; Portugal
Fil: Gatti, Daniel M.. The Jackson Laboratory; Estados Unidos
Fil: Garland, Theodore Jr. University of California; Estados Unidos
Fil: Giagia Athanasopoulou, Eva B.. Univerity of Patras; Grecia
Fil: Giménez, Mabel Dionisia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; Argentina
Fil: Grize, Sofia A.. Universitat Zurich; Suiza
Fil: Gündüz, Islam. University of Ondokuz Mayis; Turquía
Fil: Holmes, Andrew. National Institute on Alcohol Abuse and Alcoholism. Laboratory of Behavioral and Genomic Neuroscience; Estados Unidos
Fil: Hauffe, Heidi C.. Fondazione Edmund Mach; Italia
Fil: Herman, Jeremy S.. National Museums Scotland; Reino Unido
Fil: Holt, James M.. University of North Carolina; Estados Unidos
Fil: Kunjie, Hua. University of North Carolina; Estados Unidos
Fil: Jolley, Wesley J.. Island Conservation; Estados Unidos
Fil: Pardo Manuel de Villena, Fernando. University of North Carolina; Estados Unidos
Materia
MUS MUSCULUS DOMESTICUS
SELECTIVE SWEEP
SELFISH GENES
MEIOTIC DRIVE
R2d2
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/43253

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network_name_str CONICET Digital (CONICET)
spelling R2d2 drives selfish sweeps in the house mouseDidion, John P.Morgan, Andrew P.Yadgary, LiranBell, Timothy A.McMullan, Rachel C.Ortiz de Solorzano, LydiaBritton-Davidian, JaniceBult, Carol J.Campbell, Karl J.Castiglia, RiccardoChing, Yung-HaoChunco, Amanda J.Crowley, James J.Chesler, Elissa J.Förster, Daniel W.French, John E.Gabriel, Sofia I.Gatti, Daniel M.Garland, Theodore JrGiagia Athanasopoulou, Eva B.Giménez, Mabel DionisiaGrize, Sofia A.Gündüz, IslamHolmes, AndrewHauffe, Heidi C.Herman, Jeremy S.Holt, James M.Kunjie, HuaJolley, Wesley J.Pardo Manuel de Villena, FernandoMUS MUSCULUS DOMESTICUSSELECTIVE SWEEPSELFISH GENESMEIOTIC DRIVER2d2https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1A 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.Fil: Didion, John P.. University of North Carolina; Estados UnidosFil: Morgan, Andrew P.. University of North Carolina; Estados UnidosFil: Yadgary, Liran. University of North Carolina; Estados UnidosFil: Bell, Timothy A.. University of North Carolina; Estados UnidosFil: McMullan, Rachel C.. University of North Carolina; Estados UnidosFil: Ortiz de Solorzano, Lydia. University of North Carolina; Estados UnidosFil: Britton-Davidian, Janice. Université de Montpellier. Instituto Des Sciences de L'evolution; FranciaFil: Bult, Carol J.. The Jackson Laboratory; Estados UnidosFil: Campbell, Karl J.. The University Of Queensland; AustraliaFil: Castiglia, Riccardo. Universita Di Roma; ItaliaFil: Ching, Yung-Hao. University Tzu Chi. Department of Molecular Biology and Human Genetics; ChinaFil: Chunco, Amanda J.. University of North Carolina; Estados UnidosFil: Crowley, James J.. University of North Carolina; Estados UnidosFil: Chesler, Elissa J.. The Jackson Laboratory; Estados UnidosFil: Förster, Daniel W.. Leibniz - Institute for Zoo and Wildlife Research; AlemaniaFil: French, John E.. National Institute of Environmental Sciences; Estados UnidosFil: Gabriel, Sofia I.. Universidade de Lisboa; PortugalFil: Gatti, Daniel M.. The Jackson Laboratory; Estados UnidosFil: Garland, Theodore Jr. University of California; Estados UnidosFil: Giagia Athanasopoulou, Eva B.. Univerity of Patras; GreciaFil: Giménez, Mabel Dionisia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; ArgentinaFil: Grize, Sofia A.. Universitat Zurich; SuizaFil: Gündüz, Islam. University of Ondokuz Mayis; TurquíaFil: Holmes, Andrew. National Institute on Alcohol Abuse and Alcoholism. Laboratory of Behavioral and Genomic Neuroscience; Estados UnidosFil: Hauffe, Heidi C.. Fondazione Edmund Mach; ItaliaFil: Herman, Jeremy S.. National Museums Scotland; Reino UnidoFil: Holt, James M.. University of North Carolina; Estados UnidosFil: Kunjie, Hua. University of North Carolina; Estados UnidosFil: Jolley, Wesley J.. Island Conservation; Estados UnidosFil: Pardo Manuel de Villena, Fernando. University of North Carolina; Estados UnidosOxford University Press2016-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/43253Didion, John P.; Morgan, Andrew P.; Yadgary, Liran; Bell, Timothy A.; McMullan, Rachel C.; et al.; R2d2 drives selfish sweeps in the house mouse; Oxford University Press; Molecular Biology and Evolution; 33; 6; 6-2016; 1381-13950737-40381537-1719CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msw036info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/33/6/1381/2579659info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-03-31T15:06:48Zoai:ri.conicet.gov.ar:11336/43253instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-03-31 15:06:49.327CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv R2d2 drives selfish sweeps in the house mouse
title R2d2 drives selfish sweeps in the house mouse
spellingShingle R2d2 drives selfish sweeps in the house mouse
Didion, John P.
MUS MUSCULUS DOMESTICUS
SELECTIVE SWEEP
SELFISH GENES
MEIOTIC DRIVE
R2d2
title_short R2d2 drives selfish sweeps in the house mouse
title_full R2d2 drives selfish sweeps in the house mouse
title_fullStr R2d2 drives selfish sweeps in the house mouse
title_full_unstemmed R2d2 drives selfish sweeps in the house mouse
title_sort R2d2 drives selfish sweeps in the house mouse
dc.creator.none.fl_str_mv Didion, John P.
Morgan, Andrew P.
Yadgary, Liran
Bell, Timothy A.
McMullan, Rachel C.
Ortiz de Solorzano, Lydia
Britton-Davidian, Janice
Bult, Carol J.
Campbell, Karl J.
Castiglia, Riccardo
Ching, Yung-Hao
Chunco, Amanda J.
Crowley, James J.
Chesler, Elissa J.
Förster, Daniel W.
French, John E.
Gabriel, Sofia I.
Gatti, Daniel M.
Garland, Theodore Jr
Giagia Athanasopoulou, Eva B.
Giménez, Mabel Dionisia
Grize, Sofia A.
Gündüz, Islam
Holmes, Andrew
Hauffe, Heidi C.
Herman, Jeremy S.
Holt, James M.
Kunjie, Hua
Jolley, Wesley J.
Pardo Manuel de Villena, Fernando
author Didion, John P.
author_facet Didion, John P.
Morgan, Andrew P.
Yadgary, Liran
Bell, Timothy A.
McMullan, Rachel C.
Ortiz de Solorzano, Lydia
Britton-Davidian, Janice
Bult, Carol J.
Campbell, Karl J.
Castiglia, Riccardo
Ching, Yung-Hao
Chunco, Amanda J.
Crowley, James J.
Chesler, Elissa J.
Förster, Daniel W.
French, John E.
Gabriel, Sofia I.
Gatti, Daniel M.
Garland, Theodore Jr
Giagia Athanasopoulou, Eva B.
Giménez, Mabel Dionisia
Grize, Sofia A.
Gündüz, Islam
Holmes, Andrew
Hauffe, Heidi C.
Herman, Jeremy S.
Holt, James M.
Kunjie, Hua
Jolley, Wesley J.
Pardo Manuel de Villena, Fernando
author_role author
author2 Morgan, Andrew P.
Yadgary, Liran
Bell, Timothy A.
McMullan, Rachel C.
Ortiz de Solorzano, Lydia
Britton-Davidian, Janice
Bult, Carol J.
Campbell, Karl J.
Castiglia, Riccardo
Ching, Yung-Hao
Chunco, Amanda J.
Crowley, James J.
Chesler, Elissa J.
Förster, Daniel W.
French, John E.
Gabriel, Sofia I.
Gatti, Daniel M.
Garland, Theodore Jr
Giagia Athanasopoulou, Eva B.
Giménez, Mabel Dionisia
Grize, Sofia A.
Gündüz, Islam
Holmes, Andrew
Hauffe, Heidi C.
Herman, Jeremy S.
Holt, James M.
Kunjie, Hua
Jolley, Wesley J.
Pardo Manuel de Villena, Fernando
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv MUS MUSCULUS DOMESTICUS
SELECTIVE SWEEP
SELFISH GENES
MEIOTIC DRIVE
R2d2
topic MUS MUSCULUS DOMESTICUS
SELECTIVE SWEEP
SELFISH GENES
MEIOTIC DRIVE
R2d2
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Didion, John P.. University of North Carolina; Estados Unidos
Fil: Morgan, Andrew P.. University of North Carolina; Estados Unidos
Fil: Yadgary, Liran. University of North Carolina; Estados Unidos
Fil: Bell, Timothy A.. University of North Carolina; Estados Unidos
Fil: McMullan, Rachel C.. University of North Carolina; Estados Unidos
Fil: Ortiz de Solorzano, Lydia. University of North Carolina; Estados Unidos
Fil: Britton-Davidian, Janice. Université de Montpellier. Instituto Des Sciences de L'evolution; Francia
Fil: Bult, Carol J.. The Jackson Laboratory; Estados Unidos
Fil: Campbell, Karl J.. The University Of Queensland; Australia
Fil: Castiglia, Riccardo. Universita Di Roma; Italia
Fil: Ching, Yung-Hao. University Tzu Chi. Department of Molecular Biology and Human Genetics; China
Fil: Chunco, Amanda J.. University of North Carolina; Estados Unidos
Fil: Crowley, James J.. University of North Carolina; Estados Unidos
Fil: Chesler, Elissa J.. The Jackson Laboratory; Estados Unidos
Fil: Förster, Daniel W.. Leibniz - Institute for Zoo and Wildlife Research; Alemania
Fil: French, John E.. National Institute of Environmental Sciences; Estados Unidos
Fil: Gabriel, Sofia I.. Universidade de Lisboa; Portugal
Fil: Gatti, Daniel M.. The Jackson Laboratory; Estados Unidos
Fil: Garland, Theodore Jr. University of California; Estados Unidos
Fil: Giagia Athanasopoulou, Eva B.. Univerity of Patras; Grecia
Fil: Giménez, Mabel Dionisia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; Argentina
Fil: Grize, Sofia A.. Universitat Zurich; Suiza
Fil: Gündüz, Islam. University of Ondokuz Mayis; Turquía
Fil: Holmes, Andrew. National Institute on Alcohol Abuse and Alcoholism. Laboratory of Behavioral and Genomic Neuroscience; Estados Unidos
Fil: Hauffe, Heidi C.. Fondazione Edmund Mach; Italia
Fil: Herman, Jeremy S.. National Museums Scotland; Reino Unido
Fil: Holt, James M.. University of North Carolina; Estados Unidos
Fil: Kunjie, Hua. University of North Carolina; Estados Unidos
Fil: Jolley, Wesley J.. Island Conservation; Estados Unidos
Fil: Pardo Manuel de Villena, Fernando. University of North Carolina; Estados Unidos
description 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.
publishDate 2016
dc.date.none.fl_str_mv 2016-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/43253
Didion, John P.; Morgan, Andrew P.; Yadgary, Liran; Bell, Timothy A.; McMullan, Rachel C.; et al.; R2d2 drives selfish sweeps in the house mouse; Oxford University Press; Molecular Biology and Evolution; 33; 6; 6-2016; 1381-1395
0737-4038
1537-1719
CONICET Digital
CONICET
url http://hdl.handle.net/11336/43253
identifier_str_mv Didion, John P.; Morgan, Andrew P.; Yadgary, Liran; Bell, Timothy A.; McMullan, Rachel C.; et al.; R2d2 drives selfish sweeps in the house mouse; Oxford University Press; Molecular Biology and Evolution; 33; 6; 6-2016; 1381-1395
0737-4038
1537-1719
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msw036
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/33/6/1381/2579659
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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