Post on 08-Jun-2020
Many animals show intra-specific variation in body size. In some cases, there appear to be benefits of having a larger body size. For example, size is positively associatedwith improved performance,
competitiveness,andcapacitytomonopolizeresourcessuchasterritoryormatesinsomeanimals[1],andhasastrongassociationwithfemalefecundityininsects[2].Largerindividualscanalsobettercontendwith
someabiotic environmental conditions.Forexample, larger-sized individualsarebetterable tomaintain sufficientbody temperatures in colderenvironmentsandare thereforemore likely tobe foundathigher
latitudesandaltitudes, aphenomenonknownasBergmann’srule[3].However,given that large individuals requirea larger investment in termsof energyand resources,parentsarepresentedwitha trade-off
betweeninvestinginfewer,largeroffspringormore,smallerones[4,5,1].Moreover,alargerbodysizeisnotalwaysmoreadvantageous.Forexample,inhotterclimates,smallerbodysizesandlargersurfaceareato
volumeratiospromoteheatlossandcoolingbyevaporation[6].Wherethereisageneticbasistosizevariation,itmayevolvebylocaladaptation,orbyfluctuating(e.g.differentbodysizesarefavoredindifferent
yearsorseasons)orfrequency-dependent(i.e.frequency-dependentmatingsuccessorpredationofindividualsofacertainbodysize)selection.Theultimateforcesinfluencingsize-relatedfitnessintersectwiththe
underlyingproximatemechanisms thatgeneratebody size variation.Theseproximatemechanismsarevaried,butacrossdisparateanimal taxaoften involvediet and theconserved roleofnutritionalpathways,
includingtheinsulinandtargetofrapamycin(TOR)pathways[7,8],amongothermechanisms.Relationshipsbetweensizeandfitnessarethuscomplex,andbodysizedistributionsareshapedbynaturalselectionand
plasticresponsestotheenvironment.
Thebroaderproximate[7]andultimate[9]mechanismsthatshapeinsectbodysizehavebeenextensivelyreviewedelsewhere.Here,wefocusspecificallyonrecentinsightsintodriversandconsequencesof
intraspecificbodysizevariationinbees(Apoidea:Anthophila).Variationinthebodysizeofbees(Figure1)canbefoundatmanylevels:Inbothsocialandsolitaryspecies,considerablevariationisfoundwithinand
betweenpopulations,andinsocialspecies,sizevariationisalsofoundwithinandbetweencolonies[10,11].Sizevariationinbeesmayaffecttheirpollinationservices,andinsocialspeciescontributestotheirsocial
Bodysizevariationinbees:regulation,mechanisms,andrelationshiptosocialorganization
HannaChole1
SHollisWoodard2
GuyBloch1
guy.bloch@mail.huji.ac.il
1DepartmentofEcology,Evolution,andBehavior,TheAlexanderSilbermanInstituteofLifeSciences,TheHebrewUniversityofJerusalem,Jerusalem91904,Israel
2DepartmentofEntomology,UniversityofCalifornia,Riverside,Riverside,CA92521,USA
Sizepolymorphismiscommoninbees,andisdeterminedbyenvironmentalfactorssuchastemperature,broodcellsize,andthedietprovidedtodevelopinglarvae.Insocialbees,thesefactorsarefurtherinfluencedby
intricateinteractionsbetweenthequeen,workers,andthedevelopingbroodwhicheventuallydeterminethefinalsizeandcasteofdevelopinglarvae.Environmentalandsocialfactorsactinpartonjuvenilehormoneand
ecdysteroids,whicharekeyhormonal regulatorsofbodysizeandcastedetermination. In somesocialbees,bodysizevariation iscentral for socialorganizationbecause it structures reproductivedivisionof labor, task
allocationamongworkers,orboth.Atecologicalscales,bodysizealsoimpactsbee-mediatedpollinationservicesinsolitaryandsocialspeciesbyinfluencingfloralvisitationandpollinationefficacy.
CurrentOpinioninInsectScience2019,35:xx–yy
ThisreviewcomesfromathemedissueonMolecularphysiology
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https://doi.org/10.1016/j.cois.2019.07.006
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organization.
EcologicaldriversofsizevariabilityinbeesAsinotherholometabolousinsects,beebodysizeisdeterminedduringthelarvalstage,andisstronglyinfluencedbytheenvironment.Forexample,experimentalstudieshavedemonstratedthatnestmicroclimateduringearly
developmentinfluencesadultbodysizeinthemanagedsolitaryspeciesOsmiabicornis[12]andMegachilerotundata[13].Atbroaderecologicalandevolutionaryscales,thereareadditionalassociationsbetweenabioticfactorssuchas
temperatureandbeebodysizes.Mostbeespeciesstudiedsofarshowincreasesinsizewithincreasinglatitudeoraltitude.ThispatternfollowsBergmann’srule,whichiscommonbutnotuniversalininsects,andislikelyshapedby
evolutionaryprocesses[10,14••,15,9].Seasonalchangesintemperatureanddaylengthalsodrivedifferencesininsectbodysizes,includinginbees[12,9,16–18].
Bioticfactorsalsocontributetointraspecificbodysizevariation.Beesdependoverwhelminglyonfloralresourcesforfood,andtheabundanceandcompositionoftheseresources,whichchangeacrosshabitatsandseasons,are
importantdeterminantsoflarvaldiet.Inbees,asinotherinsects,dietregulatesdevelopmentandterminalbodysize,withthegeneralrulethatsmallerlarvalprovisionsgeneratesmaller-bodiedbees(describedingreaterdetailin
SectionII.‘Proximatemechanismsunderlyingbodysizevariation’).Therearealsoconsequencesofbodysizethatinfluencehowbeesextractfoodresourcesfromtheirenvironments.Bodysizeistypicallypositivelyassociatedwithforaging
range[19]andtheamountofpollenandnectar loadthebeecancarry [20,21,22••].Therefore,smaller-sized individualsmightbemoreprevalent inareaswith fewer foodresources,whereas largersizesmaybeadvantageous in
habitatswhere there is a greater need to forage at greater distances, ormaximize individual foraging loads [23]. However, being large is not always advantageous. Larger individualsmay suffer higher parasitism rates or be
preferentiallytargetedbysomepredators,forexampleinthecaseofconopidflyhostselection[24].Thereisalsoevidencesuggestingthatsmaller-sizedbumblebeesexhibithighersurvivalundersomeconditions[22••,25].
Giventheimportanceofecologicalfactorsinshapingbodysize,itisperhapsnotsurprisingthatrecentstudieshavedemonstratedthatglobalchanges,suchashabitatdegradationandlandusechange,maybedrivingchanges
inbeebodysizedistributionstowardssmallersizes.Forexample,inastudyofagroundnestingandrenid(Andrenanasonii),Renauldetal.(2006)etal.[26]foundmoresmaller-sizedbeesinareasofgreateragriculturalintensification.
Thereisalsoevidencethatoverthelastcenturyandahalf,somebeespecieshavebecomesmaller[27]andthatlarger-bodiedbeespeciesaremorelikelytohaveexhibitdeclinesinrelativeabundance[28].Theunderlyingmechanistic
driversofthesedirectionalshiftsinbeebodysizedistributionshavenotbeenexplicitlystudied,butarelikelyrelatedtothesameaforementionedenvironmentaldriversthatgeneratefluctuationsinbodysizevariation.Forexample,in
degradedorrapidlychanginghabitatsthereareoftentrendstowardsfewerfloralresources,whichmightleadtosmallerpollenmassesprovisionedinlarvalcells,whichisdirectlyrelatedtofinalbodysizeinbees(seebelowSection
II‘Proximatemechanismsunderlyingbodysizevariation’).Thisiscorroboratedbyrecentstudiesonfloweringhabitatenhancementasameanthodforbufferingthisbodysizedecline[29•].
ProximatemechanismsunderlyingbodysizevariationSolitarybees
Mostoftheworld’sbeespeciesaresolitaryandtypicallyhavelimitedabilitytoactivelyregulatetheirnestenvironment.Likeotherholometabolousinsects,allbeesgothroughseverallarvalmolts,withthefinaloneresultingin
developmentintoapupa.Giventhatpupaedonotfeed,thefinalmassofthelastlarvalinstarusuallydeterminesadultsize.Research,mostlywithfruitflies(i.e.Drosophilamelanogaster)andmoths(Manducasexta),indicatesthatbody
sizeislargelydeterminedbygrowthrateandthedurationofsensitiveperiodsduringlarvalgrowth,althoughinsomespeciesvariationinthenumberofinstarsmayalsoplayarole.Thesekeydevelopmentalfeaturesareorchestrated
bymultipleregulatoryprocessesaffectingcellgrowthandproliferation(reviewedinRef.[9]).Beeshavebeenrelativelylittleexploredinthisregard,butgiventheoverallsimilaritybetweenmothsandflies,thereiscurrentlynoreason
Figure1Bodysizevariationinbees.
A(a)BodysizevariationinthefacultativelysocialsmallcarpenterbeeCeratinacalcarata,betweenasmallworker-likesubordinatedaughter(left)andadominantreproductivemother(right)(photocreditSandraRehan).B(b)Sizepolymorphismwithin
abumblebee(Bombusterrestris)colony.Thequeenisthelargestindividualtotheleft,andallotherbeesaresisterworkersthatmayvaryinbodymassbyupto10-fold(photocreditShaiYerushalmi).C(c)Workerforager(Left)andguard(Right)ofthe
stinglessbeeTetragonisca. (undo-pleaseleavethefullnameasprovidedforthespeciesin(a)and(b))angustula.Guardsare30%heavierthanforagers(fromRef.[30••]).
alt-text:Figure1
toassumethattheorganizationprinciplesdeterminingbodysizeinbeesaresignificantlydifferent,althoughthedetailsmayvary.
Foodamount andquality are consideredamong themost important factors controllingbody size inboth solitary and social bees [20,31–34]. In insects, diet impacts growth rate,which in turn affects instar size [9]. The
microenvironment,andspecificallythetemperatureduringlarvalgrowth,isalsoimportant[35–37];Figure2).Studieswithmothsandotherinsectshaveshownthattemperaturehasapositiveeffectongrowthrate,andontherateof
biochemicalreactions,suchasJHclearing,whichaffectsthetimeofpupation[9].Inmassprovisioningsolitaryspecies,broodsizeislimitedbythesizeofthecellandthequalityorquantityofthefoodthemotherdepositsinthecell
beforeshe lays theegg.Thismaternalcontrol isperhapsbestexemplified inrecentstudiesshowing that insolitarymasonbees (Osmiaspp.spp.),pupation is triggeredwhen larvaeconsumeallpollen in thematernally-provided
provision,ratherthanwhentheyreachacriticalweight[38••,39].Insmallcarpenterbees(genusCeratina),thefirstdaughterisfedwithlessfoodandadistinctdietcomposition,andissmaller-bodiedrelativetoherlatersisters[40••].
However,itisunknownwhetherthemotherexplicitlycontrolsthedietprovisionforthefirstcell,orwhetheritsdistinctprovisionsimplyreflectsseasonalchangesinfloralresourceavailability.Studieswithhoneybeesinwhichthe
effectofcell sizeand foodprovisionedwereuncoupledsuggest thatboth factorsare important in thisspecies,but it isyetnotclearhow informationaboutcell-sizearedetectedandprocessedtoaffect the larvaldevelopmental
program[37].
Inprogressivelyprovisioningspecies,nursingadultsdynamicallycontrolthedietofdevelopinglarvaeandcanrespondtohungersignalsfromthebrood(seebelowSection II.b.1‘Thecontrolof larvaldietbytendingadults’).
Interactionsbetweentendingadultsandlarvaehavebeenstudiedmostlyinsocialinsects(discussedbelow,SectionII.b‘Socialbees’),butsimilarmechanismsarealsofoundinsomesolitarywaspsandmayalsoapplyforsolitarybees
[41].
SocialbeesThecontroloflarvaldietbytendingadults
Insocialbees,complex interactionsbetween thequeen,workers,anddevelopingbrooddetermine larvaldietandenvironment,which in turn influencedevelopmentand final size (Figure2, right). Inprogressiveprovisioners, tendingadults
dynamicallycontrollarvaldietandfeedingschedule.Themosticonicmanifestationofdiet-relatedcontroloverdevelopmentinsocial insectsisinthecaseofroyaljellyofhoneybees(Apismellifera),whichdetermineswhethera larvadevelops intoa
(larger)queenoraworker[42].Royaljellycontainsproteinsknownas‘'MajorRoyalJellyProteins'’(MRJPs),aswellasadditionalbioactivemoleculesthatareproducedintheheadglandsofnurseworkersandaffectregulatoryprocessescontrollinglarval
development[37,43–46].Forexample,aremarkablerecentfindingisthatMRJP-3actsasanextracellularRNAbindingproteinthatfacilitatesthetransferofRNAsfromworkerstolarvae[47].Thereisalsoevidencesuggestingthatphytochemicalsand
Figure2Asummaryofthefactorsaffectingbodysizeinsolitaryandsocialbees.
Bodysizevariationdependsonenvironmentalconditionsthataffectthebroodambientcondition(e.g.temperature)andfoodamountandquality.Inbothsolitaryandsocialbees,resourceavailabilityandthesizeandpositionofthelarvalcellmayinfluenceoffspringsize.In
socialbees,acomplexinterplaybetweenthequeen,theworkers,andthebrood("‘thesocialenvironment"’)determinetheambientconditions,location,cellsize,andthedietprovisionedtothedevelopinglarva,whichtogetherdetermineitsfinalbodysizeandcastefate.Notall
arrowsareapplicabletoallspeciesandtheirrelativeimportancemayvarywithspeciesecologyandlifehistorytraits.
alt-text:Figure2
smallRNAspresentinpollen,whichisonlyfedtoworker-destinedlarvae,alsoinfluencedevelopmentandcastefateinhoneybees[48,49•].ThenineMRJPsofthehoneybeeevolvedfromasingleprogenitorgeneencodingamemberoftheancientYellow
proteinfamily.ThetwosequencedbumblebeesgenomesencodeonlyasingleMRJP,suggestingthattheexpansionofthisproteinfamilyinbeesisspecifictohoneybees[50].Thereiscurrentlynoevidenceforqualitativedifferencesbetweenregurgitate
fedtoworker-destinedversusqueen-destined larvae inbumblebees [51].However, there isevidence thatdirectcontactwith thequeen impacts larvaldevelopmentalduration inB.ombusterrestris,which is consistentwith thenotion that thequeen
transferssomecurrentlyundescribedpheromonesand/orothernutritionalorbioactivemoleculestolarvae(Shpigleretal.(2013)etal.[52••],Figure3).Interestingly,thereisevidencethatdietaryhoneybeeroyaljellycanaffectdevelopmentandbodysizein
non-Apisinsects,suchasDrosophila[43]andbumblebees(Bloch,unpublishedresults).Thissuggeststhatsomeaspectsoftheregulatoryarchitectureofbodysizedeterminationaresharedbetweentheselineages,evenifupstreamdrivers(e.g.royaljelly)
differ.
RearingenvironmentSimilartosolitarybeesandotherinsects,larvaldevelopmentandtheterminalbodysizeofsocialbeesissensitivetotheenvironment.Insocialbees,thesefactorsarefurtherinfluencedbyinteractionsbetweenthequeen,workers,anddeveloping
brood.Thesumofthesefactorsisoftenreferredtoasthe‘'socialenvironment'socialenvironment’whichalsoincludescolonyage//size.Socialbeescantightlyregulatemanyaspectsofthenestmicroenvironmentthatimpactbrooddevelopmentandbodysize
(Figure2,rightpanel).Forexample,honeybeesthermoregulatetheirneststo35 ± 0.5 °CandhavestrongcontroloverotherfactorssuchashumidityandCO2levels[42].Thelocationoflarvaeinthenesthasbeenshowntoaffectbodysizeinthebumble
beeB.ombusimpatiens[53]andinthestinglessbeeTetragoniscaangustula[54]andcanbeanimportantsourceforwithin-colonyvariationinbodysize.Larvaeinthecenterofthebroodcombarefedmorefrequently,buttheymayalsobenefitfrom
improvedthermoregulationcomparedwithbrooddevelopingatthecombperiphery(butseeKelemenandDornhaus(2018)[16]forastudysuggestingthatthermoregulationissimilarinthecenterandperipheryofcoloniesofthebumblebeeB.impatiens).
Insomebumblebees,averageworkersizeincreaseswithcolonyageinawaythatisconsistentwithincreasingfoodavailabilityorbroodcarewithcolonygrowth(Fig.3)[5556,–57,52••].Across-fosteringexperimentinB.terrestris,exchanginglarvae
betweenyoungandoldcolonies,demonstratedthattheseeffectsaredrivenbytherearingcolonyenvironment,ratherthanfactorsintheegg[52••].Thus,bodysizevariationcanoriginatefromspatialortemporalvariationinresourcedistributionand,
more generally, brood care among the larvae. In addition to the location of the larvae, this distribution can also be affected by the ratio of nurse bees to larvae, and according to the task repartitionwith other duties needed, such as foraging or
thermoregulation,dependingoncolonygrowthandgeophysicalconditions[36,35,12,37,31,16,17].
InteractionswithtendingadultsthataffectbodysizeBoththequeenandtheworkersmaycontrolthelarvaldietandqualityofcare,andthiscanbeinfluencedbyinteractionsbetweenthesepartiesandwiththebrood.Forexample,inhoneybeecolonies,groupsizeandqueenpheromonesaffectthe
nurseworkerdecisionofwhethertofeedfemalelarvaewithqueenorworkerjelly[42].Thereisalsoevidencethatlarvaeinsocialspeciescommunicatetheirneedstotendingadults.Forexample,inbumblebees,cuticularpheromonescaninformabout
Figure3Aschematicself-organizedmodelfortheincreaseinworkersizeasafunctionofcolonyageinthebumblebeeBombusterrestris..terrestris.
Themodelisbasedonempiricalevidenceshowingthatlarvaethatcontactthequeenpupateearliercomparedtolarvaethataretendedbyonlyworkers,andthatthenumberoftendingworkerspositivelyaffectsthefinalsizeofthedevelopinglarva.A.(a)Schematicgraphical
modelforhowchangesinlarvaltendingbythequeenandworkersthroughoutcolonydevelopmentcandeterminebodysize.Doubledashedline:estimatedpercentageofbroodcareprovidedbythequeen.Dottedline:numberofworkersnursingthebrood.Thebluediamonds
(workers)andcircles(gynes,toprightoftheplot),showthesizeoffemalesemerginginarepresentativecolony,andthelinearregressionmodelfortheinfluenceofcolonyageonbodysize.(basedonShpigleretal2013[52]).B.(basedonShpigleretal.[52••]).(b)Summaryofknown
interactionsbetweenthequeen,theworkers,andthedevelopinglarvae.Lettersreferstothefollowingreferences:a:Blochetal.1996etal.[65],b:Bortolottietal.2001etal.[66••],c:Pereboometal.2003etal.[67],d:SmeetsandDuchateau2001[59],e:BoerandDuchateau2006[58],f:
Alauxetal.2006[68],g:Alauxetal.2007[69],h:Shpigleretal.2013[58••],f:Alauxetal.[68],g:Alauxetal.[69],h:Shpigleretal.[52••].
alt-text:Figure3
larvalhungerstate[58••],althoughtendingworkerscanvaryintheirresponsethresholdormotivationtorespondtothissignal[59].ThevolatilehoneybeebroodpheromoneE-β-ocimenealsoappearstofunctionasahungersignal,inducingworkersto
tendbroodcellsandfeedlarvae[60••].However,theinterestsofdevelopingbroodandadultsmaydiffer.Nursingadultsallocatetheirlimitedresourcesbetweenmultipledevelopingorfuturebrood,ratherthanoptimizingfoodavailabilityforasinglelarva.
Inaddition,adultsmayact inspecificwaysthat limitthesizeofthedevelopinglarvae.AninterestingexamplecomesfromPolistespaperwasps, inwhichadultsproducemechanicalsignalsthatmodulatelarvaldevelopmentandreducepropensityto
developintolargergynes[61,62].SocialinhibitionseemstoalsobeimportantinthebumblebeeB.terrestris.Inthisspecieslarvaetendedbythequeenpupateearlier,arecommonlysmaller,andarelesslikelytodevelopintogynes,comparedwithlarvae
rearedbyonlyworkers[52••,63].Queeninhibitionismediated,atleastpartially,bydirectcontactwiththequeen,andiscompromisedinlarvaeseparatedfromherbyaqueenexcluder[52••].Ascolonygroupsizesgrowlarger,moreworkersareavailable
tocareforthelarvae,andtheprobabilitythatlarvaewillbetendedbythequeendecreases(Figure3Aa).Theincreaseinworkernumberfurtheraffectsqueenbehavior,asshereducesbroodfeedingandincreasesegglaying,whichmayfurtherdiminish
herinfluenceonlarvaldevelopmentrelativetothatofworkers[64••].Theincreaseinnumberofbroodtendingbeesfurtherleadstoanincreaseinfinalbroodsize,probablybecausemoretendingworkersprovidebettercareormorefoodtothedeveloping
larvae.Figure3BbsummarizesadditionalevidenceforsocialinteractionsaffectingthedevelopmentofB.terrestrislarvae.
EndocrineandmolecularmechanismsOurunderstandingoftheendocrineandmolecularmechanismsdeterminingbodysizeinholometabolousinsectsisbasedmostlyonexperimentswithmodelspecies,suchasManducasextaandDrosophilamelanogasterM.sextaandD.melanogaster
[9,70,71].ThesestudieshaveidentifiedthecriticalroleofhormonessuchasJuvenileHormone(JH),prothoracicotropichormone(PTTH),andecdysteroids,whichtogetherorchestratethetimingofmetamorphosis,whichinturnsdictateslarvalmassat
eachmolt.ThemassofthelastlarvalinstaratwhichJHsecretionceasesanditsenzymaticbreakdownisupregulated(termedthe"criticalweight"‘criticalweight’)isthemostcriticalimportantprocessesdeterminingthetimeofpupationandthesizeofthe
emergingadult[72].Althoughtheredoesnotappeartobeacriticalweightinsomesolitarybees[38••],itiscurrentlyunknownwhetherthisdoesexistinsocialbeespecies,andhowthismightoperateinasystemwithhighlyvariableworkersizes,suchas
bumblebees.AtleastpartoftheinfluenceoftemperatureonbodysizedeterminationoccursviaitsregulationontherateofenzymaticbreakdownofJH.BodysizeincreaseswithdecreasingtemperaturebecauseofaslowrateofJHclearance,which
inducesalongerdevelopmenttimeandlargerbodysizeatpupation[12,73].Theinsulin/insulin-likegrowthfactorsignaling(IIS)pathwayisthekeypathwayslinkingnutritiontolarvalgrowthandisthereforealsoparamountfortheregulationoflarval
growthandterminalsize.
Insolitaryandsomesocialbees,sizevariationiscontinuous,whereasintheeusocialbeespecies,queensandworkerstypicallyhavenon-overlappingsizedistributions.Castedetermination,specificallyinthehighlysocialhoneybeesandstingless
bees,providessomeofthemostremarkableevidenceforpolyphenisms, theproductionof twoormoredistinctphenotypes fromthesamegenome. In insectpolyphenism,upstreamenvironmentalconditionsare integratedbythebrain,which in turn
modulatespatternsofsecretionofdevelopmentalhormonessuchasJH,ecdysteroids,andIIS.Theresultantendocrinesignalsdirectalternativedevelopmentaltrajectoriesthatleadtotheproductionofdistinctphenotypes[74•].Thesesignalingpathways
havebeenalsoimplicatedintheregulationofcastedifferentiationinthehoneybeeApis.mellifera,thebeespeciesinwhichthemechanismsunderlyingcaste-differentiationarebeststudied[75,76].Gyne-destinedhoneybeelarvaearerearedinspecial
queencellsandarefedwithadistinctiveroyaljellydiet(seeaboveSectionII.b.1.‘Thecontroloflarvaldietbytendingadults’).Subsequently,theinsulinpathwaymediatesadiet-dependentelevationinthebiosynthesisrateandcirculatinghemolymphtitersof
JH in queen-destined larvae. JH activates the expression of JH signaling genes such as Kruppel-homolog 1 (Kr-h1) andMethoprene tolerance (Met) to regulate downstream differential gene expression patterns underlying caste determination and
differentiation[75–77].JHmayalsoaffectgeneexpressionbyregulatingepigeneticprocessessuchasDNAmethylationandexpressionofmicroRNAsthathavebeenimplicatedincastedetermination[37,44–46].Castedeterminationinthehoneybee
involvesintricateprocessesotherthanthosecontrollingbodysize,andthesetopicsarebeyondthescopeofthecurrentpaper.JHandecdysteroidtitersarealsohigherinqueen-versusworker-destinedversusworker-destinedlarvae,inthebumblebeeB.
terrestris[63,78,66••](reviewedin[79]).Bortolottietal.(2001)Ref.[79]).Bortolottietal.[66••]furtherreportedthatJHtreatmentaffectslarvalgrowthandfinalbodysizeinadose-dependentandinstar-dependentmanner,withthehigherdosesappliedto
early instars resulting in development into gynes. Little is knownabout themolecular processesunderlying castedifferentiation in bumblebees, but as in honeybees, there is evidence for caste-specific expression ofmicroRNAs, suggesting their
involvementincastedifferentiation[80•].Takentogether,studiesofinsectmetamorphosis,sizedetermination,andcastedifferentiationinbeessuggestthatalloftheseprocessesareorchestratedbyinterplaybetweenJH,ecdysteroids,andIIS.Amajor
challengeforfutureresearchistounderstandhowthefine-scaletemporalmodulationofthesesameendocrinesignalingpathways(anddownstreammolecularprocesses)regulatesallthesethreepivotalprocesses.
ConsequencesofsizevariationinbeesReproductivedivisionoflaborinsocialbees
Reproductivedivisionoflaborisahallmarkofinsectsocieties,althoughthedegreeofreproductiveskewanditsrelationtobodysizedifferssignificantlyamongbeespecieswithvaryinglevelsofsocialcomplexity.Inmost
eusocialspecies,theexceedinglyfertilequeenisalsolargerthanthelessfertileworkers[81,82].Castedifferentiationcanalsoproducemorphologicalorphysiologicalvariationthatisbeyondsimplesizevariation(andthusbeyondthe
scopeofthecurrentpaper,seeSectionII.b.4‘Endocrineandmolecularmechanisms’);thesehavebeenbestexploredinthehoneybeeApis.mellifera[83],andtoalesserextentinstinglessbees[84]andbumblebees[85].
Intherelativelysmallandsimplesocietiesofsomesweatbeesandcarpenterbees,therearenodistinctfemalecastes,butthefirstfemalestoemergecanbesmallerthanlater-emergingindividuals,andonlythelatterwill
becomethefuturereproductives[36,86,87]. InthesubsocialandfacultativelysocialsmallcarpenterbeeCeratinacalcarata, largerfemalesaremorelikelytoestablishsocialnests[88•].Thefirstdaughter insocialnests is typically
smaller,non-reproductive,andbehaveslikeaworkerbyhelpingtorearhersisters,whocanpotentiallyreproducethefollowingseason(Figure1Aa)[89].Reproductivedominanceisprimarilydeterminedviaagonisticinteractionsinthe
lesscomplexinsectsocieties,wheresizecommonlycorrelateswithphysicalstrengthforwinningaggressivecontests.Agoodmodelforstudiesondominanceinteractionsisinfoundressesassociations,whichhavebeenbest-studiedin
overwinteredPolistespaperwasps[90–92],butarealsofoundinseveralbees,suchascarpenterbees(subfamilyXylocopini;e.g.,Xylocopasulcatipes,Xylocopapubescens,Ceratina.calcarata),andsweatbees(familyHalictidae;e.g.,Dialictus
lineatulus).Dominancehierarchiesarealsoimportantinqueenlessbumblebeeworkers[93].Inthesesystems,largerfemalesaremorelikelytoreproduceandlesslikelytoforage[40••,94,95].
DivisionoflaboramongstworkersinsocialspeciesMorphologicalpolymorphismispivotaltotheorganizationofworkerdivisionoflabor(knownas'alloethism'‘alloethism’)inmanyhighlysocialspecies[81].Althoughbeststudiedinthemorphologicallydistinctworkercastesof
antsandtermites,recentstudiesreportasimilarmorphologically-specializedsoldiersub-casteinseveralgeneraofstinglessbees(Figure1C;Supp.TableS1)c;SupplementaryTableS1)[30••,54].Othersocialbeespecieshaveoverall
morphologicallysimilarworkersthatvaryprimarilyinbodysize.Bumblebeesfollowthispattern,andshowthemostnotablebodysizepolymorphismamongworkers,withuptotenfoldvariabilityinmassinB.ombusterrestrisandB.
lucorum[96]andninefoldinB.impatiens[97],(Figure1B;Supp.TableS1b;SupplementaryTableS1).Largebumblebeeworkersaremorelikelytoforage,fan,andguard,thansmallerbees,whichtypicallyperformin-nestactivitiessuchas
broodtending[21,96,98–102].Larger-bodiedworkersmayalsoforageatanearlierage[98,99,102,103].Even incoloniesartificiallycomposedofonlymediumsizeworkers,andthusshowing littlesizevariability, foragerswerestill
significantlylargerthannurses,indicatingthatevensmalldifferencesinsizecanaffectthepropensitytoundertakecertaintasks[HollandandBloch,BEinrevision].Thereisevidencesuggestingthateveninhoneybees,inwhichthe
divisionoflaborrelatestoage[82],thelittlesizevariabilityamongtheworkersstillaffectstheageatwhichworkersswitchfromin-nesttoforagingactivities[104].Newgenomicstudiesinbumblebeesarebeginningtoshedlighton
underlyingdriversofthephysiologicalandbehavioraldifferencesassociatedwithworkersizepolymorphism.Forexample,thereisevidencethatsmallandlargebeesdifferinthepatternsofgeneexpression[105]andRNAediting
[106].
Beesofcertainbodysizesmaybebetterinperformingsometasks,whichcanimprovedivisionoflaborandoverallcolonyperformance.Inbumblebees,largeworkersaremoreefficientinbringingpollenandnectarbackto
thecolony[21,22••,100],andalsoappeartohavesuperiorsensorycapacities.Theyhavemoreantennalsensillaandarebetterindetectingfloralodors[107].Theircompoundeyesarealsolarger,containmoreommatidiawithalarger
facet,andhave improvedvisualdiscrimination [108].Theirocelliarealso larger,and theycan flyunder lower light intensitiescompared tosmallerworkers [109].The largereyesandocellimayalsocontribute to their stronger
phototacticresponse[110].Largebumblebeeworkersarealsobetterinsomelearningparadigms[97,111,112],havemorecircadianclockcellsintheirbrains[113],andexhibitstrongercircadianrhythms[102].Thelattermaybe
importantforsun-compassorientationandtimingvisitstoflowersattheirpeaknectarproduction.
SizepolymorphismasastrategyforoptimalresourceallocationInspiteoftheevidenceabovesuggestingthatundersomeconditionssmallbeesoutperformlargerones,theprimaryvalueofsmallerindividualsmayactuallybethereducedcostoftheirproduction.Thetrade-offbetween
offspringsizeandnumberisacommonandwell-studiedlife-historyoptimizationstrategy[4,5],andthereisevidencethatsolitarybeescanadjusttheinvestmentinoffspringtooptimizetheirfitness[39].Abumblebeecolonycan
theoretically substitute investment ina fewhighlycapable largeworkerswitha largernumberof smaller,albeit lesscompetent, individuals,whosegreaternumbersprovide insuranceagainst the lossofworkersdue todisease,
predation,orotherthreats.Resourceinvestmentstrategyisespeciallycrucialduringcolonyfoundation,whenthequeenisalone,herresourcesarestrictlylimited,andwronginvestmentdecisionscanbefatal.Ifsmallerworkersare
moreresilientagainststarvation,assuggestedbyCouvillon&Dornhaus(2010)andDornhaus[25],thentheirproductioninsuresagainstthehighresourceunpredictabilityduringcolonyfoundation.Thisearly-stagebethedgingstrategy
mayhelp inachieving the laterproductionof largerworkers,males,andgynes. Inaddition, small individuals should take less time todevelopandallow thequeen to switchearlier to investment inegg-laying rather thanbrood
provisioning[64••].Theevidencethatinmanyannualspeciesofbeesthefirstbroodofworkersiscomposedofsmallerindividualsisconsistentwiththisidea[20,32,40••,52••,88•].
SizepolymorphismandpollinationservicesBodysizemayenablebetterexploitationofavailablefloralresources.Bothacross[19]andwithin[109,114]beespecies,bodysize ispositivelyrelatedtoforagingrange,andisalsorelatedtothecapacitytocarrygreater
amountsofpollenandnectar[22••].Sizecanalsoaffectthetemporalnicheofbeesbecauseitaffectthetemperaturesinwhichbeescanbeactive,andthesizeofthecompoundeyescanaffecttheminimallightintensityandtimeof
dayunderwhichtheycanforagesuccessfully[115•].Someflowersarebetterhandledbybeesofaparticularbodysize.Forexample,tonguelengthaccountsforsomeofthevariationinflowersvisitedbylargeandsmallbumblebees,
andimpactstheefficiencyofforaginginlongversusshortcorollaflowers[11,116].However,tonguelengthsdonotnecessarilyscalewithoverallbodysizewithinbeespecies[117].Thegreaterphysicalstrengthoflargebeesmakes
thembetterinhandlingsomeflowers.Forexample,in‘tripping’,theinsect'slegsandthoraxexposetheanthersandstigmaoftheflower[10].Inbuzzpollination,beesholdaflower'’santhersandvibrateatacertainfrequencyinorder
toextractthepollen[118•],andheretoo,bodysizeappearstobeimportantinrespecttoamplitude[119•]orfrequency[120•].Thereisalsoevidencethatsomeflowersarebetterhandledbysmallbees[121].Insomestinglessbees,
suchasMeliponaquadrifasciata[20]andM.eliponaflavolineata[122],smallerforagershavelargercorbiculaerelativetotheirbodysizeandareabletocarryheavierloadsofpollenperunitofbodycomparedwithlargerindividuals[20].In
socialbees,size-variableindividualsofthesamespeciescanpollinateabroaderrangeofflowerspecieswithinthesamehabitat[10,11,123],makingthemkeystonepollinatorsinmanypollinationnetworks.
SummaryandfuturedirectionsBodysizevariationiscommoninbees,andcanbefunctionallysignificantforbothsolitaryandsocialspecies.Giventhesometimesconflictinganddynamiccostsandbenefitsofbodysize,itisnotsurprisingthatbodysizeisnot
alwayspositivelycorrelatedwithhighfitnessinbees[124–128].Asinotheranimals,itisassumedthattheinvolvementofmultiplefactorsonbodysizeleadstostabilizingselection,whereselectivepressuresandtrade-offsfavoring
largerversussmallersizesarebalancedwithinpopulations [1]. Insocialbeessuchasbumblebees,bodysizepolymorphismmaybe important forsocialorganizationbecause it influences twoof themost importantorganization
principlesofinsectsocieties:reproductivedivisionoflaborbetweenqueensandworkers,andvariationintaskperformanceamongworkers.Thus,notsurprisingly,insomesocialinsectstheregulationofbodysizeisunderstrong
social influence, inways thatwe are only beginning to understand. In both solitary and social bees, there are significantmaternal influences on brood development through control of diet composition, the brood cell, and the
microenvironment(Figure2),),andalsofeedingrateintheprogressively-provisioningspecies.Thesituationismorecomplexinsocialbees,inwhichbrooddevelopmentisinfluencedbyintricateinteractionsbetweenthebrood,the
motherqueen,andtheworkers.Animportantvenueforfutureresearchistounderstandhowthedifferentpartiesacttomeettheirinterests,specificallyincasesofconflictrelatedtobodysize.Tounderstandthesecomplexsystems,
wewillneedtobetterunderstandcommunicationbetweentheseinteractingparties,includingthechemicalandfunctionalcharacterizationofhungersignals,andtheways,inwhichtendingadultsresponsedtothem.Muchresearchis
alsoneededtoidentifythespecificnutrientsorbioactivemoleculesthatplayaroleinsizedetermination.Identificationofthesesignalswillallowustounderstandhownutritionalandsocialfactorsactonthemolecularpathwaysthat
regulatelarvaldevelopmentandultimatebodysize.Fromabroaderevolutionaryperspective,comparativestudiesonthesepathwaysacrossdifferentbeelineagesandacrosslevelsofsocialcomplexitywillshedlightonhowbodysize
evolvesasafunctionofsociality,whichisanoverlookedaspectoftheevolutionofinsectsociality.
ReferencesandrecommendedreadingPapersofparticularinterest,publishedwithintheperiodofreview,havebeenhighlightedas:
•ofspecialinterest
••ofoutstandinginterest
AcknowledgementsThisworkwassupportedbyresearchgrantsfromtheUS–IsraelBinationalScienceFoundation(BSFBSF;toG.B.andS.H.W.),theUS–IsraelBinationalAgriculturalResearchandDevelopmentFund(BARDBARD;
toG.B.andS.H.W.),TheNationalAcademiesKeckFuturesInitiative(NAKFI;toG.B),andUSDAUSDANIFA(toS.H.W.).
AppendixA.SupplementarydataSupplementarymaterialrelatedtothisarticlecanbefound,intheonlineversion,atdoi:https://doi.org/10.1016/j.cois.2019.07.006.
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QueriesandAnswersQuery:Theauthornameshavebeentaggedasgivennamesandsurnames(surnamesarehighlightedintealcolor).Pleaseconfirmiftheyhavebeenidentifiedcorrectly.Answer:CholeWoodardBloch
Query:Pleasecheckwhetherthedesignatedcorrespondingauthoriscorrect,andamendifnecessary.Answer:GuyBlochisthecorrespondingauthor,hise-mailiscorrect
Query:Fullnames(includingfullfirstname,noinitials)aremandatoryforallauthors.Pleaseprovidethefullfirstnamefortheauthor‘SHollisWoodard’.Answer:SarahHollisWoodard
Query:Pleasecheckthee-mailaddressforthecorrespondingauthorthathasbeenaddedhere,andcorrectifnecessary.Answer:Itiscorrect
Query:Highlightsmustbeprovidedas3–5bulletpoints,eachbulletpointhavingamaximumof125characters.Pleaserephrasethefollowinghighlightsorprovidenewhighlights.Answer:Insocialbees,larvaldevelopmentandfinalsizearealsodeterminedbyintricateinteractionsbetweenthequeen,workers,andbrood
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AppendixA.SupplementarydataThefollowingisSupplementarydatatothisarticle:
MultimediaComponent1
Highlights
• Bodysizevariationiscommoninsolitaryandsocialbees.
• Insolitaryspecies,larvalgrowthiscontrolledbydietandtheabioticenvironment.
• Insocialbees,larvaldevelopmentandfinalsizeisarealsodeterminedbyintricateinteractionsbetweenthequeen,workers,andthedevelopingbrood.
• Bodysizestructuresdivisionoflaborinsomebees.
• Bodysizemayinfluenceforaging,floralhandling,andpollinationservicesatecosystemscales.
Query:Thischeckthe4thhighlightpointforclarityandamendifnecessary.Answer:Bodysizeinfluencesdivisionoflaborinsomesocialbees.
Query:Pleasesupplyashorttitleof80charactersorfewer(includingspaces)andthatdoesnotcontainanyabbreviations.Answer:Bodysizevariationinbees
Query:Pleaseprovidetheexpansionforgenusname‘B.lucorum’.Answer:weexpandthefirstB.toBombus,itisclearthatthefollowingonesareofthesamegenus
Query:Asperjournalstylesheet’ConflictofIntereststatement’shouldbepublishedbothinPDFandScienceDirect.KindlydownloadandfilltheCOIformfromhttps://www.elsevier.com/declaration-of-competing-interestsandsubmititalongwiththecorrections.Answer:Done.Theauthorsdeclarethattheyhavenoknowncompetingfinancialinterestsorpersonalrelationshipsthatcouldhaveappearedtoinfluencetheworkreportedinthispaper.Attachments:declaration-of-competing-interestsGB.docx
Query:Havewecorrectlyinterpretedthefollowingfundingsource(s)andcountrynamesyoucitedinyourarticle:BSF,BARD,NationalAcademiesKeckFuturesInitiative,USDA?Answer:Yes
Query:PleaseprovidethevolumenumberandpagerangeforthebibliographyinRefs.29•,70,81,86,110,119•,120•?Answer:Ref29:inpress?Ref70:Pages207-218inL.B.Martin,C.K.Ghalambor,andH.A.Woods,eds.Intergrativeorganismalbiology.Wiley,Hoboken,NJ.Ref81562pages.Ref86:volume46pages359-423.Ref110:bioRxiv.Ref119:2019inpress.Ref120:9(8):4875-4887.
Query:PleasechecktheeditsmadeinRef.103andamendifnecessary.Answer:Fine