Anarchy Is a Molecular Signature of Worker Sterility in the Honey Bee.
Identifieur interne : 002330 ( PubMed/Checkpoint ); précédent : 002329; suivant : 002331Anarchy Is a Molecular Signature of Worker Sterility in the Honey Bee.
Auteurs : Isobel Ronai [Australie] ; Benjamin P. Oldroyd [Australie] ; Deborah A. Barton [Australie] ; Guénaël Cabanes [France] ; Julianne Lim [Australie] ; Vanina Vergoz [Australie]Source :
- Molecular biology and evolution [ 1537-1719 ] ; 2016.
Descripteurs français
- KwdFr :
- MESH :
- génétique : Abeilles, Infertilité, Mort cellulaire, Ovogenèse.
- physiologie : Abeilles.
- Animaux, Comportement social, Femelle.
English descriptors
- KwdEn :
- MESH :
- genetics : Bees, Cell Death, Infertility, Oogenesis.
- physiology : Bees.
- Animals, Female, Social Behavior.
Abstract
Worker sterility is a defining characteristic of eusociality. The existence of the sterile worker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant "anarchistic" strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation. We quantified the expression of the four most promising candidate genes (Anarchy, Pdk1, S6k, and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2% accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a "gene underlying altruism". When we knocked down expression of Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death. Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first example of a gene that has evolved through kin selection to regulate worker sterility.
DOI: 10.1093/molbev/msv202
PubMed: 26416979
Affiliations:
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Oldroyd</name><affiliation wicri:level="4"><nlm:affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, The University of Sydney, Sydney, NSW</wicri:regionArea><orgName type="university">Université de Sydney</orgName><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Barton, Deborah A" sort="Barton, Deborah A" uniqKey="Barton D" first="Deborah A" last="Barton">Deborah A. Barton</name><affiliation wicri:level="4"><nlm:affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, The University of Sydney, Sydney, NSW</wicri:regionArea><orgName type="university">Université de Sydney</orgName><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Cabanes, Guenael" sort="Cabanes, Guenael" uniqKey="Cabanes G" first="Guénaël" last="Cabanes">Guénaël Cabanes</name><affiliation wicri:level="4"><nlm:affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia Institut Galilée, Université Paris 13, Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia Institut Galilée, Université Paris 13, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement><settlement type="city">Sydney</settlement></placeName><orgName type="university">Université de Sydney</orgName></affiliation></author><author><name sortKey="Lim, Julianne" sort="Lim, Julianne" uniqKey="Lim J" first="Julianne" last="Lim">Julianne Lim</name><affiliation wicri:level="4"><nlm:affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, The University of Sydney, Sydney, NSW</wicri:regionArea><orgName type="university">Université de Sydney</orgName><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Vergoz, Vanina" sort="Vergoz, Vanina" uniqKey="Vergoz V" first="Vanina" last="Vergoz">Vanina Vergoz</name><affiliation wicri:level="4"><nlm:affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, The University of Sydney, Sydney, NSW</wicri:regionArea><orgName type="university">Université de Sydney</orgName><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author></analytic><series><title level="j">Molecular biology and evolution</title><idno type="eISSN">1537-1719</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Bees (genetics)</term><term>Bees (physiology)</term><term>Cell Death (genetics)</term><term>Female</term><term>Infertility (genetics)</term><term>Oogenesis (genetics)</term><term>Social Behavior</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Abeilles (génétique)</term><term>Abeilles (physiologie)</term><term>Animaux</term><term>Comportement social</term><term>Femelle</term><term>Infertilité (génétique)</term><term>Mort cellulaire (génétique)</term><term>Ovogenèse (génétique)</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Bees</term><term>Cell Death</term><term>Infertility</term><term>Oogenesis</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Abeilles</term><term>Infertilité</term><term>Mort cellulaire</term><term>Ovogenèse</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Abeilles</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Bees</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Female</term><term>Social Behavior</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Comportement social</term><term>Femelle</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Worker sterility is a defining characteristic of eusociality. The existence of the sterile worker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant "anarchistic" strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation. We quantified the expression of the four most promising candidate genes (Anarchy, Pdk1, S6k, and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2% accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a "gene underlying altruism". When we knocked down expression of Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death. Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first example of a gene that has evolved through kin selection to regulate worker sterility.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26416979</PMID><DateCreated><Year>2015</Year><Month>12</Month><Day>30</Day></DateCreated><DateCompleted><Year>2016</Year><Month>09</Month><Day>27</Day></DateCompleted><DateRevised><Year>2015</Year><Month>12</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1537-1719</ISSN><JournalIssue CitedMedium="Internet"><Volume>33</Volume><Issue>1</Issue><PubDate><Year>2016</Year><Month>Jan</Month></PubDate></JournalIssue><Title>Molecular biology and evolution</Title><ISOAbbreviation>Mol. Biol. Evol.</ISOAbbreviation></Journal><ArticleTitle>Anarchy Is a Molecular Signature of Worker Sterility in the Honey Bee.</ArticleTitle><Pagination><MedlinePgn>134-42</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/molbev/msv202</ELocationID><Abstract><AbstractText>Worker sterility is a defining characteristic of eusociality. The existence of the sterile worker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant "anarchistic" strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation. We quantified the expression of the four most promising candidate genes (Anarchy, Pdk1, S6k, and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2% accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a "gene underlying altruism". When we knocked down expression of Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death. Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first example of a gene that has evolved through kin selection to regulate worker sterility.</AbstractText><CopyrightInformation>© The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ronai</LastName><ForeName>Isobel</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia isobel.ronai@sydney.edu.au.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oldroyd</LastName><ForeName>Benjamin P</ForeName><Initials>BP</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barton</LastName><ForeName>Deborah A</ForeName><Initials>DA</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cabanes</LastName><ForeName>Guénaël</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia Institut Galilée, Université Paris 13, Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lim</LastName><ForeName>Julianne</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vergoz</LastName><ForeName>Vanina</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>09</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Biol Evol</MedlineTA><NlmUniqueID>8501455</NlmUniqueID><ISSNLinking>0737-4038</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001516" MajorTopicYN="N">Bees</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007246" MajorTopicYN="N">Infertility</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009866" MajorTopicYN="N">Oogenesis</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012919" MajorTopicYN="N">Social Behavior</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">anarchy</Keyword><Keyword MajorTopicYN="N">honey bee</Keyword><Keyword MajorTopicYN="N">oogenesis</Keyword><Keyword MajorTopicYN="N">ovary activation</Keyword><Keyword MajorTopicYN="N">programmed cell death</Keyword><Keyword MajorTopicYN="N">worker sterility</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2015</Year><Month>9</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2015</Year><Month>9</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>9</Month><Day>28</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">26416979</ArticleId><ArticleId IdType="pii">msv202</ArticleId><ArticleId IdType="doi">10.1093/molbev/msv202</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Australie</li><li>France</li></country><region><li>Nouvelle-Galles du Sud</li><li>Île-de-France</li></region><settlement><li>Paris</li><li>Sydney</li></settlement><orgName><li>Université de Sydney</li></orgName></list><tree><country name="Australie"><region name="Nouvelle-Galles du Sud"><name sortKey="Ronai, Isobel" sort="Ronai, Isobel" uniqKey="Ronai I" first="Isobel" last="Ronai">Isobel Ronai</name></region><name sortKey="Barton, Deborah A" sort="Barton, Deborah A" uniqKey="Barton D" first="Deborah A" last="Barton">Deborah A. Barton</name><name sortKey="Lim, Julianne" sort="Lim, Julianne" uniqKey="Lim J" first="Julianne" last="Lim">Julianne Lim</name><name sortKey="Oldroyd, Benjamin P" sort="Oldroyd, Benjamin P" uniqKey="Oldroyd B" first="Benjamin P" last="Oldroyd">Benjamin P. Oldroyd</name><name sortKey="Vergoz, Vanina" sort="Vergoz, Vanina" uniqKey="Vergoz V" first="Vanina" last="Vergoz">Vanina Vergoz</name></country><country name="France"><region name="Île-de-France"><name sortKey="Cabanes, Guenael" sort="Cabanes, Guenael" uniqKey="Cabanes G" first="Guénaël" last="Cabanes">Guénaël Cabanes</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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