Pheromones affecting ovary activation and ovariole loss in the Asian honey bee Apis cerana

PheromonesaffectingovaryactivationandovariolelossintheAsian

honeybeeApis

cerana

KenTana,b,XiwenLiub,SihaoDongb,ChaoWangb,BenjaminP.Oldroydc,⇑

aKeyLaboratoryofTropicalForestEcology,XishuangbannaTropicalBotanicalGarden,ChineseAcademyofScience,Kunming,YunnanProvince650223,ChinabEasternBeeResearchInstituteofYunnanAgriculturalUniversity,Heilongtan,Kunming,YunnanProvince650201,ChinacBehaviourandGeneticsofSocialInsectsLaboratory,SchoolofBiologicalSciencesA12,UniversityofSydney,NSW2006,Australia

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Articlehistory:Received4December2014Receivedinrevisedform9January2015Accepted12January2015Availableonline20January2015

Keywords:PrimerpheromoneQueenmandibularpheromone9-Keto-(E)-2-decenoicacid(9-ODA)(E)-10-hydroxy-2-decenoicacid(10-HDA)10-Hydroxydecanoicacid(10-HDAA)Signallingabstract

TheAsianhivebeeApisceranahassimilarqueenmandibularpheromones(QMP)totheWesternhoneybeeApismellifera.HowevertheeffectsofindividualQMPcomponentshaveneverbeentestedtodeter-minetheireffectsonthereproductivephysiologyofA.ceranaworkers.WefedonequeenequivalentofeachofthemajorcomponentsofA.ceranaQMPtogroupsofc.a.500day-old,caged,workerstwiceadayuntiltheworkerswere10daysold.Halfofthecageswerealsoprovidedwith10%royaljellyinthefood.Workersweresampledeachdayanddissectedtodeterminethenumberofovariolesandthedegreeofovaryactivation(eggdevelopment).Incagestreatedwith9-carbonfattyacidsovaryactivationwasminimal,whereasthe10-carbonacidssuppressedovaryactivationverylittle.Royaljellyenhancedovaryactivation,especiallyincagestreatedwith10-carbonacids.Thenumberofovariolesdeclinedwithbeeage,buttherateofdeclinewasslowedbythe9-carbonacidsinparticular.Theresultsshowconser-vationofthecompositionandfunctionofQMPbetweenA.ceranaandA.melliferaandsupportthehypothesisthatQMPisanhonestsignalofqueenfecundityratherthanachemicalcastratorofworkers.Ó2015ElsevierLtd.Allrightsreserved.

1.Introduction

WorkersofeusocialHymenopteransaregenerallysterileinthe

presenceofaqueen.However,inmanyspeciesworkersretain

functionalovaries,whichtheyactivateiftheirqueenislost,pro-

ducingviableoffspringmalesbyarrhenotokousparthenogenesis.

Facultativeworkersterilityofthiskindrequiresthatworkerscan

detectthepresenceoftheirqueen,andmodifytheirreproductive

physiologyappropriatelyifsheislost.Inallspeciesstudiedthus

far,queenssignaltheirpresenceandregulateworkerovaryactiva-

tionviaprimerpheromones(Dietemannetal.,2005;Hooveretal.,

2003;LeConteandHefetz,2008;LimandLee,2005;van

Oystaeyenetal.,2014;VargoandHulsey,2000).

Cuticularhydrocarbonsarelongchainalkanes,alkenesand

methyl-branchedhydrocarbonswhoseprimaryandoriginalfunc-

tionistoprotectinsectsfromdesiccation(Blomquist,2010).How-

everinmostsocialHymenopteranscuticularhydrocarbonshave

beenco-optedtoplayaroleinqueensignaling(Liebig,2010;

Nunesetal.,2014;vanOystaeyenetal.,2014).Queenandworkerhydrocarbonprofilesdiffer,andthisprovidesworkerswitha

mechanismtodetectthepresenceofaqueenintheircolony

(Liebig,2010).Amajorexceptiontothisgeneralityisthehoney

bees,genusApis,wherethequeen’ssignalisamixtureoflong-

chainfattyacidssecretedfromthemandibularglands(Butler,

1959;Plettneretal.,1997;Slessoretal.,2005).Thesepheromones

inhibitworkerovaryactivation(Hooveretal.,2003),mediate

workerretinueformationaroundthequeen(Slessoretal.,1988),

andactasasexattractant(Gary,1962).

Workerhoneybeesalsoproducepheromonesfromtheirman-

dibularglands,butthesediffersignificantlyfromthoseofqueens.

Inthecavity-nestinghoneybeesApisceranaandApismellifera,

mandibularglandsecretionsofqueenshaveahighproportionof

9-keto-(E)-2-decenoicacid(9-ODA),whereasthesecretionsof

queenrightworkersarericherin(E)-10-hydroxy-2-decenoicacid

(10-HDA)and10-hydroxydecanoicacid(10-HDAA)(Keeling

etal.,2001;Plettneretal.,1997).Thustheratioof9-HDA+9-

ODA/10-HDA+10-HDAAisameasureoftherelative‘queenliness’

ofthepheromonalsignal(Hooveretal.,2005;Moritzetal.,2000),

andthemore9-ODAcirculatinginacolony,thelesslikelyA.melli-

feraworkersaretoactivatetheirovaries(Hooveretal.,2003).The

mandibularsecretionsofqueenrightA.ceranaworkershave

extremelylowamountsof9-ODAandarelativelyhighproportion

of9-HDA(Plettneretal.,1997;Tanetal.,2012).HoweverwhenA.

http://dx.doi.org/10.1016/j.jinsphys.2015.01.0060022-1910/Ó2015ElsevierLtd.Allrights

reserved.⇑Correspondingauthor.Tel.:+61293517501.E-mailaddresses:kentan@xtbg.ac.cn(K.Tan),liuxiwen1345890@163.com(X.Liu),850143087@qq.com(S.Dong),402615976@qq.com(C.Wang),benjamin.oldroyd@sydney.edu.au(B.P.

Oldroyd).JournalofInsectPhysiology74(2015)25–29

ContentslistsavailableatScienceDirect

JournalofInsectPhysiology

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