Empirical evidence for son-killing X chromosomes and the operation of SA-zygotic drive
Diploid organisms have two copies of all genes, but only one is carried by each haploid gamete and diploid offspring. This causes a fundamental genetic conflict over transmission rate between alternative alleles. Single genes, or gene clusters, only rarely code for the complex phenotypes needed to g...
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| description | Diploid organisms have two copies of all genes, but only one is carried by each haploid gamete and diploid offspring. This causes a fundamental genetic conflict over transmission rate between alternative alleles. Single genes, or gene clusters, only rarely code for the complex phenotypes needed to give them a transmission advantage (drive phenotype). However, all genes on a male's X and Y chromosomes co-segregate, allowing different sex-linked genes to code for different parts of the drive phenotype. Correspondingly, the well-characterized phenomenon of male gametic drive, occurring during haploid gametogenesis, is especially common on sex chromosomes. The new theory of sexually antagonistic zygotic drive of the sex chromosomes (SA-zygotic drive) extends the logic of gametic drive into the diploid phase of the lifecycle, whenever there is competition among siblings or harmful sib-sib mating. The X and Y are predicted to gain a transmission advantage by harming offspring of the sex that does not carry them.
Here we analyzed a mutant X-chromosome in Drosophila simulans that produced an excess of daughters when transmitted from males. We developed a series of tests to differentiate between gametic and SA-zygotic drive, and provide multiple lines of evidence that SA-zygotic drive is responsible for the sex ratio bias. Driving sires produce about 50% more surviving daughters than sons.
Sex-ratio distortion due to genetic conflict has evolved via gametic drive and maternally transmitted endosymbionts. Our data indicate that sex chromosomes can also drive by harming the non-carrier sex of offspring. |
| doi_str_mv | 10.1371/journal.pone.0023508 |
| format | Article |
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Here we analyzed a mutant X-chromosome in Drosophila simulans that produced an excess of daughters when transmitted from males. We developed a series of tests to differentiate between gametic and SA-zygotic drive, and provide multiple lines of evidence that SA-zygotic drive is responsible for the sex ratio bias. Driving sires produce about 50% more surviving daughters than sons.
Sex-ratio distortion due to genetic conflict has evolved via gametic drive and maternally transmitted endosymbionts. Our data indicate that sex chromosomes can also drive by harming the non-carrier sex of offspring.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0023508</identifier><identifier>PMID: 21858149</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Algorithms ; Analysis ; Animals ; Biological evolution ; Biology ; Chromosomes ; Competition ; Diploidy ; Disease transmission ; Drosophila ; Drosophila melanogaster ; Drosophila simulans ; Ecology ; Empirical analysis ; Endosymbionts ; Evolution ; Female ; Gametogenesis ; Gametogenesis - genetics ; Gene clusters ; Gene expression ; Genes ; Genes, Insect - genetics ; Genetic aspects ; Haploidy ; Inheritance Patterns ; Insects ; Life cycle analysis ; Male ; Males ; Marine biology ; Microorganisms ; Models, Genetic ; Mutation ; Offspring ; Phenotypes ; Selection, Genetic ; Sex ; Sex chromosomes ; Sex Factors ; Sex linkage ; Sex Ratio ; Sperm ; Spiroplasma ; Wolbachia ; X Chromosome - genetics ; X chromosomes ; Y Chromosome - genetics ; Y chromosomes ; Zygote - metabolism</subject><ispartof>PloS one, 2011-08, Vol.6 (8), p.e23508-e23508</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Friberg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Friberg et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c766t-957a5c9f3fa2cba5cbc33eebe95054f2de980b5769bd6f1b8f6f2994c72b781c3</citedby><cites>FETCH-LOGICAL-c766t-957a5c9f3fa2cba5cbc33eebe95054f2de980b5769bd6f1b8f6f2994c72b781c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3157394/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3157394/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21858149$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:liu:diva-137218$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-158594$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Imhof, Axel</contributor><creatorcontrib>Friberg, Urban</creatorcontrib><creatorcontrib>Stewart, Andrew D</creatorcontrib><creatorcontrib>Rice, William R</creatorcontrib><title>Empirical evidence for son-killing X chromosomes and the operation of SA-zygotic drive</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Diploid organisms have two copies of all genes, but only one is carried by each haploid gamete and diploid offspring. This causes a fundamental genetic conflict over transmission rate between alternative alleles. Single genes, or gene clusters, only rarely code for the complex phenotypes needed to give them a transmission advantage (drive phenotype). However, all genes on a male's X and Y chromosomes co-segregate, allowing different sex-linked genes to code for different parts of the drive phenotype. Correspondingly, the well-characterized phenomenon of male gametic drive, occurring during haploid gametogenesis, is especially common on sex chromosomes. The new theory of sexually antagonistic zygotic drive of the sex chromosomes (SA-zygotic drive) extends the logic of gametic drive into the diploid phase of the lifecycle, whenever there is competition among siblings or harmful sib-sib mating. The X and Y are predicted to gain a transmission advantage by harming offspring of the sex that does not carry them.
Here we analyzed a mutant X-chromosome in Drosophila simulans that produced an excess of daughters when transmitted from males. We developed a series of tests to differentiate between gametic and SA-zygotic drive, and provide multiple lines of evidence that SA-zygotic drive is responsible for the sex ratio bias. Driving sires produce about 50% more surviving daughters than sons.
Sex-ratio distortion due to genetic conflict has evolved via gametic drive and maternally transmitted endosymbionts. Our data indicate that sex chromosomes can also drive by harming the non-carrier sex of offspring.</description><subject>Algorithms</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Chromosomes</subject><subject>Competition</subject><subject>Diploidy</subject><subject>Disease transmission</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila simulans</subject><subject>Ecology</subject><subject>Empirical analysis</subject><subject>Endosymbionts</subject><subject>Evolution</subject><subject>Female</subject><subject>Gametogenesis</subject><subject>Gametogenesis - genetics</subject><subject>Gene clusters</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genes, Insect - genetics</subject><subject>Genetic aspects</subject><subject>Haploidy</subject><subject>Inheritance Patterns</subject><subject>Insects</subject><subject>Life cycle analysis</subject><subject>Male</subject><subject>Males</subject><subject>Marine biology</subject><subject>Microorganisms</subject><subject>Models, Genetic</subject><subject>Mutation</subject><subject>Offspring</subject><subject>Phenotypes</subject><subject>Selection, Genetic</subject><subject>Sex</subject><subject>Sex chromosomes</subject><subject>Sex Factors</subject><subject>Sex linkage</subject><subject>Sex Ratio</subject><subject>Sperm</subject><subject>Spiroplasma</subject><subject>Wolbachia</subject><subject>X Chromosome - 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This causes a fundamental genetic conflict over transmission rate between alternative alleles. Single genes, or gene clusters, only rarely code for the complex phenotypes needed to give them a transmission advantage (drive phenotype). However, all genes on a male's X and Y chromosomes co-segregate, allowing different sex-linked genes to code for different parts of the drive phenotype. Correspondingly, the well-characterized phenomenon of male gametic drive, occurring during haploid gametogenesis, is especially common on sex chromosomes. The new theory of sexually antagonistic zygotic drive of the sex chromosomes (SA-zygotic drive) extends the logic of gametic drive into the diploid phase of the lifecycle, whenever there is competition among siblings or harmful sib-sib mating. The X and Y are predicted to gain a transmission advantage by harming offspring of the sex that does not carry them.
Here we analyzed a mutant X-chromosome in Drosophila simulans that produced an excess of daughters when transmitted from males. We developed a series of tests to differentiate between gametic and SA-zygotic drive, and provide multiple lines of evidence that SA-zygotic drive is responsible for the sex ratio bias. Driving sires produce about 50% more surviving daughters than sons.
Sex-ratio distortion due to genetic conflict has evolved via gametic drive and maternally transmitted endosymbionts. Our data indicate that sex chromosomes can also drive by harming the non-carrier sex of offspring.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21858149</pmid><doi>10.1371/journal.pone.0023508</doi><tpages>e23508</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Algorithms Analysis Animals Biological evolution Biology Chromosomes Competition Diploidy Disease transmission Drosophila Drosophila melanogaster Drosophila simulans Ecology Empirical analysis Endosymbionts Evolution Female Gametogenesis Gametogenesis - genetics Gene clusters Gene expression Genes Genes, Insect - genetics Genetic aspects Haploidy Inheritance Patterns Insects Life cycle analysis Male Males Marine biology Microorganisms Models, Genetic Mutation Offspring Phenotypes Selection, Genetic Sex Sex chromosomes Sex Factors Sex linkage Sex Ratio Sperm Spiroplasma Wolbachia X Chromosome - genetics X chromosomes Y Chromosome - genetics Y chromosomes Zygote - metabolism |
| title | Empirical evidence for son-killing X chromosomes and the operation of SA-zygotic drive |
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