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Sexual dimorphism in Diabrotica speciosa and Diabrotica viridula (Coleoptera: Chrysomelidae)

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RevistaBrasileiradeEntomologia62(2018)172–175

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

w w w . r b e n t o m o l o g i a . c o m

Short

Communication

Sexual

dimorphism

in

Diabrotica

speciosa

and

Diabrotica

viridula

(Coleoptera:

Chrysomelidae)

Mayara

De

Carli

a

,

Caroline

Rech

a

,

José

Maurício

Simões

Bento

b

,

Cristiane

Nardi

a,∗

aUniversidadeEstadualdoCentro-Oeste(UNICENTRO),DepartamentodeAgronomia,Guarapuava,PR,Brazil

bUniversidadedeSãoPaulo,EscolaSuperiordeAgricultura“LuizdeQueiroz”(ESALQ),DepartamentodeEntomologiaeAcarologia,Piracicaba,SP,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received16February2018 Accepted24April2018 Availableonline5May2018 AssociateEditor:AdrianaMarvaldi Keywords:

Morphology Rootworms Sexualbehavior

a

b

s

t

r

a

c

t

Diabroticaspeciosa(Germar)andDiabroticaviridulaF.(Coleoptera:Chrysomelidae)arethetwomost abundantspeciesofthegenusinSouthAmerica,andbelongtothefucataandvirgiferagroups,respectively. Here,wecharacterizethedimorphismofthesetaepresentonthebasitarsiofmalesandfemalesofthese species.Dimorphismwasconfirmedinbothspecies,anditwasrelatedtothepresenceofadhesivesetae exclusivelyinmales,whichpossessthesestructuresonthebasaltarsomeresofthepro-andmesothoracic legs.

©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

SexualdimorphisminspeciesofDiabroticaChevrolathasbeen indicatedasanimportantfeatureusefulinmorphologic,taxonomic andphylogeneticstudies(Cabreraetal.,2008;CabreraandCabrera Walsh,2010;MohamedsaidandFurth,2011;Prado,2013).Besides theshapeofabdominaltipsandthelengthofantennomeres2and3 inmales,theadhesivesetaeofmesothoracicandmetathoraciclegs contributetoseparatethesexesinsomespecies(Cabreraetal., 2008;CabreraandCabreraWalsh,2010;Gloynaetal.,2014).

InSouthAmerica,thepredominantspeciesisDiabroticaspeciosa (Germar),followedbyD.viridulaF.AlthoughD.speciosaisthemost abundantandmostdamagingtoagriculturalcrops,D.viridulahas expandedsignificantlyfromnorthernArgentinaintosoutheastern Brazil(CabreraWalsh,2003).Inthepresentwork,westudiedthe morphologyofthelegsofmalesandfemalesofD.speciosaandD. viridula,inordertocharacterizetheadhesivesetaeasafeatureto separatethesexesinthosespecies.

Themorphologicalanalysiswasperformedafterremovalofthe prothoracic,mesothoracicandmetathoraciclegsofmale(N=4)and female(N=4)specimensofD.speciosaandD.viridula.Thetypesof setaepresentonthetarsomeresandthelengthofthesurfacethat theyoccupiedwereanalyzed.

Setaeofthefilamentous,lanceolate,spatulateanddiscoidtypes wereobservedbyusingalightmicroscopyanddescribedaccording tothenomenclatureadoptedbyGloynaetal.(2014).

∗ Correspondingauthor.

E-mail:nardicris@gmail.com(C.Nardi).

Diabrotica speciosa and D. viridula show sexual dimorphism associated withthe basaltarsomeres ofthepro-and mesotho-raciclegs.Thesespecieshavesimilartypesandpatternsofsetaeon theprotarsus,mesotarsusandmetatarsus.InfemalesofD.speciosa andD.viridula,thefirstandsecondtarsomeresoftheprothoracic, mesothoracicandmetathoraciclegsarecoveredwithfilamentous setae;thethirdtarsomereiscoveredwithlanceolatesetaeonthe basalthird and withspatulatesetaeontheapicalthird.Fourth and fifth tarsomeres covered sparsely with filamentous setae (Figs.1and2).

InmalesofD.speciosaandD.viridula,theprothoraciclegshave discoidsetae,covering90%(0.241mm)and96%(0.282mm) respec-tivelyoftherectangulararea,fromthebasetotheapicalregionof thefirsttarsomere.Themarginsofthispatcharesetwith lance-olateandfilamentoussetae(Table1,Figs.1and2).Atthebaseof themesothoraciclegs,60%(0.206mm)and40%(0.119mm) respec-tively,ofthefirsttarsomereiscoveredwithanovalpatchofdiscoid setae,bordered bylanceolatesetae;theapicalthird of the tar-somereiscoveredwithfilamentoussetae(Table1,Figs.1and2). Theremainingtarsomeresofthepro-andmesothoraciclegsand thoseofthemetathoraciclegspresentsimilartypesand arrange-mentsofsetaeasthoseoftheD.speciosaandD.viridulafemales (Table1).

As shown for D. virgifera virgifera Le Conte (Hammack and French,2007),D.collicola(CabreraandCabreraWalsh,2010)and other genera of Diabroticites and Phyllectrites (Cabrera, 1999; CabreraandCabrera Walsh,2004;Moura,2010),wefoundthat this dimorphism also occurs in the South American species

https://doi.org/10.1016/j.rbe.2018.04.004

0085-5626/©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

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M.DeCarlietal./RevistaBrasileiradeEntomologia62(2018)172–175 173

Prothoracic Mesothoracic Metathoracic

500 µm 200 µm 200 µm 500 µm Male 500 µm 500 µm S L F F emale F F F S L F F L S L L L S S S F F F F F F D D

Fig.1.Prothoracic,mesothoracicandmetathoraciclegsofmaleandfemaleofDiabroticaviridula,showingthesexualdimorphisminthebasaltarsomereofthepro-and mesothoraciclegs.Setae:D,discoid;F,filamentous;L,lanceolate;S,spatulate.

Table1

Length(mm)(±standarddeviation)oftarsomerssurfacecoveredbyeachtypeofsetaeofDiabroticaspeciosaandD.viridulamalesandfemales.

Species Sex Leg Setaeonthesurfaceoftarsomers

I II III IV+V

Filamentous Discoid Filamentous Lanceolated+Spatulated Filamentous

D. speciosa Female Prothoracic 0.257±0.02 – 0.173±0.02 0.133±0.03 0.236±0.01 Mesothoracic 0.328±0.03 – 0.209±0.03 0.157±0.01 0.248±0.02 Metathoracic 0.476±0.09 – 0.242±0.00 0.146±0.02 0.302±0.05 Male Prothoracic 0.025±0.00 0.241±0.04 0.208±0.01 0.140±0.01 0.247±0.02 Mesothoracic 0.131±0.02 0.206±0.05 0.224±0.02 0.128±0.01 0.262±0.01 Metathoracic 0.527±0.04 – 0.232±0.04 0.173±0.02 0.277±0.04

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174 M.DeCarlietal./RevistaBrasileiradeEntomologia62(2018)172–175 Table1(Continued)

Species Sex Leg Setaeonthesurfaceoftarsomers

I II III IV+V

Filamentous Discoid Filamentous Lanceolated+Spatulated Filamentous

D. viridula Female Prothoracic 0.288±0.04 – 0.205±0.02 0.187±0.01 0.315±0.04 Mesothoracic 0.354±0.03 – 0.208±0.03 0.181±0.02 0.340±0.03 Metathoracic 0.552±0.04 – 0.262±0.03 0.197±0.02 0.368±0.05 Male Prothoracic 0.01±0.00 0.282±0.05 0.183±0.03 0.165±0.02 0.284±0.03 Mesothoracic 0.180±0.07 0.119±0.04 0.171±0.02 0.179±0.03 0.286±0.03 Metathoracic 0.509±0.01 – 0.255±0.04 0.170±0.01 0.331±0.06

Prothoracic Mesothoracic Metathoracic

200µm 200µm 200µm 200µm 200µm 500µm Male S S L F F emale F F F L F F L S L L L S S S F F F F F D D D

Fig.2.Prothoracic,mesothoracicandmetathoraciclegsofmaleandfemaleofDiabroticaspeciosa,showingthesexualdimorphisminthebasaltarsomereofthepro-and mesothoraciclegs.Setae:D,discoid;F,filamentous;L,lanceolate;S,spatulate.

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M.DeCarlietal./RevistaBrasileiradeEntomologia62(2018)172–175 175 D.speciosaandD.viridula,withadhesivesetaepresentexclusively

inmales.

Thespecializationofthetarsusforthesexualfunctionhasbeen describedpreviouslyforchrysomelids,especiallywithregardtoa tarsusthatisdilatedatthebase(Crowson,1981)andthediscoid tipsof thesetae(Stork, 1983).The adhesivenatureof thetarsi ofmalesofD.speciosaand D.viridula,provided bythepatchof shortdiscoidsetae,isprobablyrelatedtosexualbehavior.Nardi etal.(2012)demonstratedthatmalesofD.speciosasupport them-selvesontheelytraofthefemalesduringpre-copula,copulaand post-copula.ThissexualbehaviorwasalsoobservedinD.virgifera virgiferaand D. barberiSmith& Lawrence(Lewand Ball, 1979; Medvedevand Pavlov,1988; Tallamy et al.,2003).In addition,

HammackandFrench(2007)reportedthatmalesrubthebasitarsi ofthepro-and mesothoraciclegsontheelytraof thefemales, whichmaintaintheminapositionabovethefemales.Inviewof theimportanceattributedtothemorphologyofthebasitarsusof males,itisimportanttodeterminewhethertheareaprovidedwith discoidsetaevariesin sizeindifferentindividuals,which could influencetheeffectivenessanddurationofcopulation,male–male competitionandsexualselection,culminatinginanincreaseinthe reproductivesuccessofmaleswithlargeradhesivepatches. There-fore,thesizeofthepatchofdiscoidsetaewouldbe,besidethebody size(FrenchandHammack,2014),anadditionalfactorin intraspe-cificcompetition.In thisrespect,Katsukietal.(2014),studying SagrafemorataDrury (Chrysomelidae),observedthat thesexual dimorphisminmalemetathoraciclegshasimplicationsfor male-malecompetitionandsexualselection.Thissuggestionemphasizes theimportanceforthegenusofthisdimorphisminthebasitarsus. Besidesotherrelatedstudieswhichdescribeattributesto dis-tinguishthe sexesin Diabroticina (Prado, 2013), our findingof adhesivesetae,presentinmalesofD.speciosaandD.viridula,also contributetotheknowledgeofsexuallydimorphiccharactersin thisgroup.

Funding

ThisworkwassupportedbyNationalInstituteofScienceand Technology– Semiochemicalsin Agriculture[FAPESPandCNPq –grants#2014/50871-0and#465511/2014-7,respectively];and CNPq[Universalgrants#460390/2014-7].

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

We are grateful to Dr. Paulo Rogério Pinto Rodrigues, Dr. Tiago Sawczen (Ambiotec/Unicentro) for helping in the MEV analysis and Dr. Diego B. Silva for improvement of the manuscript.

References

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CabreraWalsh,G.,2003.HostrangeandreproductivetraitsofDiabroticaspeciosa (Germar)andDiabroticaviridula(F.)(Coleoptera:Chrysomelidae),twospecies ofSouthAmericanpestrootworms,withnotesonotherspeciesofDiabroticina. Environ.Entomol.32,276–285.

Cabrera,N.,CabreraWalsh,G.,2004.Platybroticamisionensisanewgenusand speciesofLuperini(Coleoptera:Chrysomelidae:Galerucinae)fromArgentina. Ann.Entomol.Soc.Am97,6–14.

Cabrera,N.,Sosa-Gómez,D.,Michelim,A.,2008. Morphologicalandmolecular characterizationofanewspeciesofDiabrotica(Coleoptera,Chrysomelidae, Galerucinae).Zootaxa1922,33–48.

Cabrera,N.,CabreraWalsh,G.,2010.Diabroticacollicola(Coleoptera:Chrysomelidae) anewspeciesofleafbeetlefromArgentinaandkeytospeciesoftheDiabrotica virgiferagroupandrelatives.Zootaxa2683,45–55.

Crowson,R.A.,1981.TheBiologyoftheColeoptera.AcademicPress,London. French,B.W.,Hammack,L.,2014.Malereproductivecompetitionandcomponents

offemalefitnessinrelationtobodysizeinnortherncornrootworm(Coleoptera: Chrysomelidae).Ann.Entomol.Soc.Am.107,279–287.

Gloyna,K.,Thieme,T.,Gorb,S.,Voigt,D.,2014.Newresultsonsexualdifferences intarsaladhesivesetaeofDiabroticavirgiferavirgiferaLeConte(Coleoptera, Chrysomelidae,Galerucinae).Eur.J.Environ.Sci.4,97–101.

Hammack,L.,French,B.W.,2007.Sexualdimorphismofbasitarsiinpestspeciesof DiabroticaandCerotoma(Coleoptera:Chrysomelidae).Ann.Entomol.Soc.Am. 100,59–63.

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Lew,A.C.,Ball,H.J.,1979.Thematingbehaviorofthe.westerncornrootworm Dia-broticavirgifera(Coleoptera:Chrysomelidae).Ann.Entomol.Soc.Am.72,15. Medvedev, L.N., Pavlov, S.I., 1988. Mating behavior of the Chrysomelidae

(Coleoptera).Entomol.Rev.67,100–108.

Mohamedsaid, M.S.,Furth,D.G.,2011. Secondary sexual characteristicsinthe Galerucinae(sensustricto)(Coleoptera:Chrysomelidae).ISRNZool.2011,1–61. Moura,L.,2010.Coronabrotica,anewgenusandspeciesofLuperini,andakeyto gen-eraofSectionPhyllecthrites(Coleoptera,Chrysomelidae,Galerucinae).Zootaxa 2675,26–32.

Nardi,C.,Luvizotto,R.A.,Parra,J.R.P.,Bento,J.M.S.,2012.Matingbehaviorof Diabrot-icaspeciosa(Coleoptera:Chrysomelidae).Environ.Entomol.41(3),562–570. Prado,L.R.,2013.Reviewontheuseofsexuallydimorphiccharactersinthe

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