全 文 ：ActaZootaxonomicaSinica, 36 (1):1-11(Jan.2011)
动物分类学报
ISSN1000-0739
ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(30830017), NationalScienceFundsforDistinguishedYoungScientists
(31025024), NationalScienceFundforFosteringTalentsinBasicResearch(J0930004), agrant(O529YX5105)fromtheKeyLaboratoryoftheZoological
SystematicsandEvolutionoftheChineseAcademyofSciences, ShanghaiNaturalScienceFoundation(10ZR1408500), andtheMinistryofScienceand
TechnologyofthePeoplesRepublicofChina(2006FY110500).
＊Correspondingauthor, E-mail:qiaogx@ioz.ac.cn
Received25Sep.2010, accepted10Dec.2010.
1
MORPHOLOGICALADAPTATIONOFAPHIDSPECIESFEEDINGONDIFFERENTSITESOFPOPULUS
FANGYan1, 2 , HUANGXiao-Lei1 , QIAOGe-Xia1＊ , ZHANGGuang-Xue1
1.KeyLaboratoryofZoologicalSystematicsandEvolution, InstituteofZoology, ChineseAcademyofSciences, Beijing　100101, China
2.SchoolofLifeScience, EastChinaNormalUniversity, Shanghai　 200062, China
Abstract　Inordertounderstandmorphologicaladaptationofaphidstodistinctgaltypesandfeedingsitesofrelatedhost
plants, morphologicalvariationsof122 fieldclonesfromtenaphidspecieswithdifferentgaltypesandfeedingsitesonPopulus
werestudiedusinggeneraldescriptivestatistics, canonicalvariatesanalysis(CVA)andclusteringanalysisbasedon
morphometrics.CVAsandclusteringanalysisbothrevealedthatmorphologicaldifferencesof122 clonesfromtenaphid
specieswereassociatedwiththegaltypesandfeedingsitesonhostplants.Thescoresofthefirsttwocanonicalvariates
(CVs)clearlyseparatedthegaldwellersfromfreeliversinthefirstCVA, separatedthetruegaldwellersfrompseudo-gal
dwelersbothonleavesdistinctlyinthesecondCVA, andprovidedevidentseparationamongdiferentfeedingsitesoffree
liversinthefinalCVA.Generalstatisticalanalysiswithmeasurementsofultimaterostralsegments, tarsiandclawsfurther
supportedtheseparations.Clearlyseparationsofaphidclonesofdifferentspeciescorrespondingtodifferentgaltypesand
feedingsitesonthehostplantandvariationsofmorphologicalcharactersamongdifferentclustersofaphidssuggest
morphologicaladaptationfortheaphidspeciestodiferentgaltypesandfeedingsitesonPopulus.Possiblereasonsfor
morphologicalvariationsamongdiferentaphidclusterswerediscussed.Itwasalsosuggestedthatthestudyonconstructing
phylogenyandtraditionaltaxonomyofinsectsbymorphologymustconsidermorphologicaladaptations, andthestudyon
insect-hostplantrelationshipmusttakeaccountofcombinedmorphologicalcharactersandotherinfluentialfactors.
Keywords　Aphids, feedingsites, galtypes, morphologicaladaptation, Populus.
1　Introduction
Amongaboutonemilionknowninsectspeciesin
theworld, halfofthem wereherbivorous(Qin,
1987). Mostofphytophagousinsectsfeed and
reproduceonthesurfacesoftheirhostplantsduring
theirwholelifecycles(Moran, 1986).Insectsacquireaseriesofvarietiesonmorphologicalfeaturestoadapt
tohostplantsurfaces(Peeters, 2002), thenatureof
theplantsurfaceisone ofthe factorscausing
morphological adaptations, some kinds ofmorphologicaladaptationshavecertainlybeennoted
(Bernays, 1991).Now, variationsofmorphological
characters can be analysed quantitatively,morphologicaladaptations can be elucidated by
statisticalanalysis.
Aphidoidea ( Insecta, Sternorrhyncha,
Hemiptera)areagroupofsap-suckinginsects, whicharecloselyrelatedwiththeirhostplants.Thereare
morethan4 700 knownaphidspeciesworldwide, and
theirhostplantsbelongto2 120 genera, 267 families.Feedingsitesofaphidsshowhighdiversity, suchas
leaves, youngtwigs, stems, inflorescences, rootsand
fruits(Fangetal., 2006a).Somestudiesshowedthat
someaphidcharactersvariedwithdiferentsurface
traitsofhostplantleaves.Thetarsallength of
TuberculoidesannulatusHartigandMyzocalisschreiberiHileRisLambers＆ Stroyandiferedfrom eachother
significantly, becausethesetwoaphidspeciesfedon
diferentleafsubstrates, roughorsmooth, oftwo
respective hostplants which belong to Quercus(Kennedy, 1986).ForUroleuconspecies, thelengthof
hindtarsiwassignificantlynegativelycorrelatedwith
thetrichomedensityofleavesfordiferenthostplants(AsteraceaeandCampanulaceae), aswelasthe
lengthoftheultimaterostralsegmentswaspositively
correlatedwiththetrichomedensity(Moran, 1986).
Incontrast, somecharactersofdiferentaphidspecieswerevariedlitleamongtheleavesofkindsofclosely
relatedhostplantswhich theywerefeedingon.
Morphologicalcharacters, especialy the ultimaterostralsegments, thetarsiandtheclawsoftheaphids
feedingon leavesofthecloselyrelatedbamboos
showedhighsimilarity(Fangetal., 2006b).Thisconvergenceindicated morphologicaladaptation of
diferentaphidstotherelatedhostplantsandsame
sites.However, morphologicaladaptationofaphids
feedingondiferentsitesofhostplantshasnotbeenstudiedbefore.Thepresentstudyselectedtenaphid
ActaZootaxonomicaSinica动物分类学报 Vol.36　No.1
speciesfeedingondiferentsitesoftherelatedhost
plantsPopulusformorphologicalanalysis.
Diferentsitesofcertainhostplantspossessverydiferentfeatures, thesurfaceandinnerstructuresor
tissuesamongleaf, petiole, twig, stem, barkandroot
werediferent(Li, 1984).Populusarepopularhostplantsforaphids.Populusareagroupofloftydefoliated
arbores, whichcontainmorethan100 speciesinthe
world(Ma, 2003), mainlydistributeontemperate
zoneand frigid zone, asEurope, Asia, NorthAmerica, MiddleEastand thecountriesaround
MediterraneanSea.TheaphidsfeedingonPopulus
belongto33 generaof7subfamilies, thecountsarealthesecondmostongenericorsubfamiliallevelof
aphids(BlackmanandEastop, 1994;Remaudièreand
Remaudière1997;Fangetal., 2006a).Aphidsfeeding
onPopulusarerestrictedtodiferentsites.Inaddition,someaphidsofEriosomatinaecaninducegalson
petioles, leaves, shootsandotherpartsofpoplars
(Zhangetal., 1999).Basedonabovestudies, wepresumedthatthemorphologicalcharactersofaphids
mightvaryamongdiferentgalformationsorfeeding
sitesofrelatedhostplantsandthedistinctvarieties
mightindicatetheaphidmorphologicaladaptation.Here, aphidson diferentsitesofPopulus, with
diferentgaltypes(gal, pseudo-galorno-gal)were
selectedandtheirquantitativedatawereusedforstatisticanalysistotestourassumption.
2　MaterialsandMethods
2.1　Aphidspecies
Thestudywasbasedonmaterials(permanent
slides)fromthecolectionsoftheZoologicalMuseumatInstituteofZoology, ChineseAcademyofSciences
(ZMCAS)consistingofsamplesfromdiferentregions
ofChinawhichwerecolectedduringlastsixdecades
(Table1).Fieldaphidsampleswithdistincttabs(diferentcolectiondatesandlocalities)treatedas
variousclones, thatoneclone contained aphids
colectedfromnearsitesofonehostplantindividualatonetime.Thestudiedmaterialsconsistedof122clones
(732 aphidindividuals)offieldsamplesbelongingto
tenaphidspecies, fivesubfamilies, whichfedon
diferentsitesofPopulus, suchasleaf, petiole, twig,stemandbark, someoftheminducedgalsorpseudo-
gals.Inapreliminaryanalysisofthemorphological
measurements, wefound thatvaluesofselectedcharactermeasurementsforalateandapterousmorphs
onChaitophoruswerealmostsame(byindependentt-
test;P > 0.05), and Phloeomyzuspaserini and
Pterocomma neimogolensewere with few alate fieldsamples, so weexamined adultalateviviparous
femalesformostspeciesexceptPh.paseriniandPt.
neimogolense, whichwerewithapterae.
2.2　Selectionandmeasurementofcharacters
Aphidswerecolectedfrom thehostplantsand
preservedin75% or100% ethanolinthefield, thenbringtolaboratory formountingon slides.The
methodswasfolowedZhangandZhong(1983),
BlackmanandEastop(2000).FootitandMackquer(1990)foundthatthe
measurementsofmorphologicalcharactersbetweenthe
rightandtheleftsideoftheaphidbody, suchas
lengthofantennaeorlegs, didnotdifersignificantly(bypairedt-test;P>0.05).Sothesidewithgood-
shapedofeachindividualwasmeasured.Butsome
width measurementswerevaried asa resultofdistortionfromtheslide-mountingprocedure(Footit
andMackquer, 1980), sothewidthmeasurementwas
onlytakenfromnormalposeindividuals.
Usualy, 2 - 11 specimens (minimum 2,maximum29)ofeachfieldsampleweremeasured.
Thecharactersmeasuredandtheirabbreviationswere
listedinTable2 (fordetailsofmeasurementsseeZhangandZhong, 1983;IlharcoandvanHarten,
1987).Almeasurementswerecarriedoutwitha
phase contrastmicroscope (LeitzDIZLUX 20,
Germany)usingacalibratedmicrometereyepiece.
2.3　Statisticalanalysis
Generaldescriptivestatisticswereruntoexplore
thetraitsofthedatamatrix.Themeans, standard
deviation(SD), andcoeficientofvariability(CV)formorphometricswithdiferentaphidspeciesfrom
clonemeanswerecalculated.
Toexaminewhetherhostpositionsandgalstate-relateddiferenceexistedamongfieldsamples, the
wholedataweresubmitedtoacanonicalvariates
analysis(CVA)withoutanypriordatatransformation
(Albrecht, 1980;Reymentetal., 1984).Thenthedatawasseparatedintotwopartsbygalstates, andof
eachpartweresubmitedtosubsequentCVAs.Inal
analysis, diferentclones/fieldsamplestreatedasgroupfactors.
TheMahalanobisdistancesbetween fivegal
dwelingspeciesfrommorphometricsof11 characters
of74 fieldcloneswerecalculated, andthenclusteringanalysiswasusedtoexaminemorphologicalvariations
amongthefivespecies.Theclusteringanalysiswas
implemented by Wards method. At last, thedendrogramofthefiveaphidspecieswasoutput.
CVA wasperformedusingSps 13.0 (Spss,
Inc.)statisticalpackageandclusteringanalysiswas
performedusingStatistica6.0 (Statsoft, Inc.).
2.4　 Mapfeedingsitesand galtypesontheclusteringdendrogram
Hostplantrelatedtraitsoffeedingsitesandgal
typesweremappedontheclusteringdendrogram inordertodiscusthemorphologicaladaptationofthefive
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Jan.2011 方　燕等:蚜虫对杨属植物不同寄生部位的形态适应
　Table1.Therelatedinformationof122 aphidclonesfor10 aphidspecies.
Subfamily Species Feedingsite Gal No. Measured Date Location
Chaitophprinae Chaitophorus
populeti
(Panzer, 1801)
Undersurface
ofleaves,
petiole,
twig
No 82 5 29May1948 China, Beijing
25 3 June1956 China, Henan(Anyang)
8 29Apr.1957 China, Henan(Anyang)
4 19May1957 China, Henan(Huixian)
2 27June1957 China, Liaoning(Xiongyue)
4 11May1962 China, Beijing
2 15June1962 China, Beijing
11 16June1972 China, Hebei(Yixian)
10 20June1972 China, Shandong(Qingdao)
2 June1975 China, Shandong(Qingdao)
4 5 June1978 China, Hebei(Shunyi)
2 8 June1961 China, Xinjiang
3 19June1984 China, Hebei(Shexian)
Chaitophorus
populialbae
(Boyerde
Fonscolombe,
1841)
Undersurface
ofleaves
No 31 5 29Apr.1957 China, Henan(Anyang)
15 8 Oct.1963 China, Beijing
2 Sep.1975 China, Shandong(Yantai)
3 20May1977 China, Beijing(Sanpu)
4 26Sep.1983 China, Hebei(Baoding)
2 7 May1984 China, Hebei(Handan)
Hormaphidinae Dorsphispopuli
(Maskel,
1898)
Undersurfaceof
leaves, few
onuppersurface
No 72 13 16June1972 China, Hebei(Yixian)
3 4 June1978 China, Yunnan(Kunming)
29 19May1980 China, Yunnan(Xiaguan)
24 30May1980 China, Yunnan(Lijiang)
3 Apr.1987 China, Shandong(Taishan)
Eriosomatinae Epipemphigus
imaicus
(Cholodkovsky,
1912)
Undersurface
ofleaves
Yes
Pseudo
71 12 29May1976 China:Beijing(Sanpu)
16 15May1980 China, Yunnan(Kunming)
5 19May1980 China, Yunnan(Jianchuan)
25 21May1980 China, Yunnan(Lijiang)
3 13May1981 China, Guizhou(Guiyang)
4 29July1981 China, Xizhang(Yadong)
2 24June1983 China, Xizang(NamlinXian)
4 3 July1983 China, Xizhang(NamlinXian)
Pemphigusborealis
Tulgren, 1909
Branch Yes 95 3 23June1957 China, Jilin(Jiuzhan)
5 30June1972 China, Beijing(Sanpu)
6 29May1976 China, Beijing(Sanpu)
5 17July1976 China, Heilongjiang(Keshan)
12 18July1976 China, Heilongjiang(KedongXian)
6 14Oct.1976 China, Yunnan(Kunming)
4 19May1977 China, Beijing(Shahe)
9 8 June1978 China, Beijing(Sanpu)
5 15May1980 China, Yunnan(Kunming)
10 16May1980 China, Yunnan(Kunming)
4 1 June1980 China, Yunnan(Dali)
2 16June1980 China, Yunnan(Dongchuan)
2 23July1980 China, Yunnan(Luoci)
2 23July1980 China, Yunnan(Xiaguan)
2 30Oct.1982 China, Yunnan(Kunming)
2 15July1985 China, Hebei(Chicheng)
4 21July1999 China, Gansu(Wenxian)
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ActaZootaxonomicaSinica动物分类学报 Vol.36　No.1
　ContinueTable1.
Subfamily Species Feedingsite Gal No. Measured Date Location
Eriosomatinae Pemphigusborealis
Tulgren, 1909
Branch Yes 95 4 21July1999 China, Gansu(Wenxian)
4 21July1999 China, Gansu(Wenxian)
4 21July1999 China, Gansu(Wenxian)
Pemphigus
immunis
Buckton, 1896
Baseoftwig Yes 111 6 30May1957 China, Henan(Anyang)
4 23July1957 China, Jilin(Gongzhuling)
5 23July1957 China, Jilin(Gongzhuling)
6 2 July1960 China, Ningxia(Yinchuan)
6 4 July1961 China, Liaoning(Shenyang)
11 12June1962 China, Beijing
15 8 June1962 China, Beijing
2 22June1970 China, Hebei(Dacheng)
4 20June1974 China, Beijing(Fangshan)
8 28June1976 China, Heilongjiang(Haerbin)
5 5 Aug.1979 China, Beijing
9 1 July1980 China, Liaoning(Chaoyang)
3 13June1983 China, Hebei(Xinglong)
5 10June1984 China, Hebei(Shexian)
6 30June1984 China, Hebei(Xiaowutai)
7 18July1985 China, Liaoning(Fuxin)
4 31Aug.1986 China, NeiMongol(Chifeng)
5 7 July1987 China, NeiMongol(Chifeng)
Pemphigus
matsumurai
Monzen, 1929
Uppersurfaceof
leaves(baseof
petiole)
Yes 80 4 23June1957 China, Jilin(Jiuzhan)
2 15July1974 China, Ningxia(Yinchuan)
7 27May1975 China, Beijing(Sanpu)
11 27May1975 China, Beijing(Yuling)
7 8 June1978 China, Beijing(Sanpu)
2 20June1979 China, Beijing(Badaling)
9 16May1980 China, Yunnan(Kunming)
4 25May1980 China, Yunnan(Lijiang)
4 13June1983 China, Beijing(Badaling)
2 3 July1983 China, Hebei(Kangbao)
5 7 July1983 China, Xizang(Renbung)
4 18June1984 China, Hebei(Xiaowutai)
7 19June1984 China, Hebei(Xiaowutai)
4 18June1986 China, Hebei(Zhuolu)
4 1 July2002 China, Xizang(Büba)
4 29June2003 China, Beijing
Pemphigus
tibetensis
Zhang, 1979
Twigs(baseof
petiole)
Yes 65 10 9 Sep.1973 China, Xizang(Bomi)
8 8 Sep.1978 China, Beijing(Sanpu)
3 25Oct.1978 China, Xizang(Qamdo)
2 11Sep.1979 China, Xizang(Lhasa)
11 5 Sep.1979 China, Beijing(BotanicalGarden)
10 5 Sep.1979 China, Beijing(Sanpu)
4 5 Spe.1979 China, Beijing(Sanpu)
6 19Nov.1979 China, Beijing(Badaling)
3 27June1982 China, Yunnan(Lufeng)
2 23Aug.2003 China, Xizang(Lhasa)
2 23Aug.2003 China, Xizang(Lhasa)
4 22Aug.2005 China, Xizang(Zayǜ)
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　ContinueTable1.
Subfamily Species Feedingsite Gal No. Measured Date Location
Phloeomyzinae Phloeomyzus
paserini
(Signoret,
1875)
Crevicesof
stem, under
bark, evenon
roots
No 71 2 1 Jan.1956 China, Jilin(Gongzhuling)
5 8 Aug.1964 China, Hebei(Xiaowutai)
7 June1975 China, Shandong(Qingdao)
2 11July1975 China, Beijing(Badaling)
3 10June1976 China, Beijing(Sanpu)
2 16June1976 China, Heilongjiang(Keshan)
6 21June1976 China, NeiMongol(Hohhot)
5 19July1976 China, Heilongjiang(Suihua)
6 19July1978 China, Beijing(Sanpu)
7 28Sep.1979 China, Beijing(Sanpu)
6 1 July1980 China, Liaoning(Chaoyang)
2 18June1981 China, Shandong(Qingdao)
6 11July1982 China, Liaoning(Shenyang)
7 5 July1983 China, Hebei(Zhangbei)
3 26July1984 China, Hebei(Chongli)
2 28July1984 China, Hebei(Chongli)
Pterocommatinae Pterocomma
neimogolense
Zhang, 1980
Twig, culm No 54 9 21June1976 China, NeiMongol(Hohhot)
3 22May1983 China, Liaoning(Shenyang)
6 30Apr.1985 China, Hebei(Cixian)
6 30Apr.1985 China, Hebei(Cixian)
9 2 Apr.1985 China, Hebei(Raoyang)
16 4 Oct.1986 China, Gansu(Minxian)
3 29Sep.1986 China, Gansu(Minxian)
2 5 Oct.1987 China, Gansu(Zhangye)
　 Table 2. Continuousvariablesmeasured with their
abbreviations.
Abbreviation Variable
Ursl Ultimaterostralsegment, length
Ursw Ultimaterostralsegment, basalwidth
Ftil Foreleg, tarsalsegmentⅠ , length
Ftil Foreleg, tarsalsegmentⅡ , length
Mtil Midleg, tarsalsegmentⅠ , length
Mtil Midleg, tarsalsegmentⅡ , length
Htil Hindleg, tarsalsegmentⅠ , length
Htil Hindleg, tarsalsegmentⅡ , length
Fcl Foreleg, claw, length
Mcl Midleg, claw, length
Hcl Hindleg, claw, length
galdwelingaphidspeciestothesurfaceofdiferent
hostplantsitesandgaltypes.
3　Results
3.1　Descriptiveanalysisofmorphologicalcharacters
Themean, SD andCV of11 charactersfor
diferentaphidspeciesareshowninTable3.The
resultsshowedthatthemeanvaluesofcharacter
measurementsofaphidswerenotalwayscloseinonegenus, andwerediversewithinvariousrangesfor
diferentgenera, suchastherangeofmeansof
ultimaterostralsegmentslengthfortwoChaitophorus
speciesis0.061mm, fromC.populeti(0.185mm)toC.populialbae(0.124 mm);itwaslargerthanthe
range(0.028 mm)offourPemphigusspecies, P.
borealis(0.096 mm), P.immunis(0.080 mm), P.matsumurai(0.108mm)andP.tibetensis(0.090mm).
TheCVofalmorphometricsforeachaphidspecies
rangedfrom 1.13 % to13.56 %.TheCVoffore
(1.13%-7.62%), middle(2.37%-7.91%)andhind(2.63% -8.30 %)firsttarsalsegmentslength
fordiferentaphidspeciesweremuchlower, andthe
CVofultimaterostralsegmentlength(3.20 % -
12.65%), ultimaterostralsegmentwidth(4.01%-
12.51 %), clawlengthofmiddlelegs(1.38 % -
13.56%)andclawlengthofhindlegs(3.53 % -
11.09%)fordiferentaphidspecieswerehigherthanothers.TheCVvaluesofmiddlefirsttarsalsegments
length(2.37 % -7.91 %)fordiferentspecies
showedarelativelynarowrange, whereasofclawlengthofmiddlelegs(1.38%-13.56%)waswitha
widerrange.
3.2　CVAanalysis
Intheanalysisofthe122 fieldclones, thefirst
twoCVstogetheraccountedfor89.6 % ofthetotalvariationinthedata(Table4).ScoresonCV1
separatedtheclonesintotwomainclusters(Fig.1).
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Jan.2011 方　燕等:蚜虫对杨属植物不同寄生部位的形态适应
　Table4.Canonicalcoefficients(standardized)andpercentagesoftotalvarianceaccountedbyvectorswhichcontributedtotheseparationsoftheaphidclonesexaminedbythethreecanonicalvariatesanalysis(CVAs)performed.
Variables FirstCVA(Fig.1) SecondCVA(Fig.2 ) ThirdCVA(Fig.3)
1　 2　 1　 2　 1　 2　
Ursl -0.920 0.561 0.601 -0.392 -0.620 1.033
Ursw 0.009 0.053 -0.070 0.072 0.171 -0.151
Ftil -0.093 -0.020 -0.151 0.064 -0.041 0.039
Ftil 0.192 0.205 0.159 -0.040 0.429 0.029
Mtil -0.155 -0.073 -0.223 -0.060 0.039 0.004
Mtil 0.271 0.418 0.336 -0.123 0.580 0.115
Htil -0.067 -0.286 -0.257 -0.104 -0.122 -0.285
Htil 0.490 0.185 0.378 -0.094 0.397 -0.046
Fcl 0.135 0.054 0.055 0.461 -0.019 -0.024
Mcl 0.142 0.064 0.119 0.618 0.107 -0.064
Hcl 0.033 0.085 0.118 0.422 0.103 0.063
%oftotalvariance 66.8 22.8 63.1 9.2 69.5 26.7
　　Note.SeeTable2fornamesofvariables.
Oneclustercontainedmostofthegaldwelercloneswhiletheotherincluded freelivingclones.The
morphologicalcharacterscontributingmostto the
separationofthetwoclusters(i.e.thatwiththe
highestcanonicalcoeficientsforCV1) wastheultimaterostralsegmentlengthandhindsecondtarsal
segmentlength(Table4).Thescoresonthefirsttwo
CVscouldnotseparatetheclonesofdiferentfeedingsitesclearly(plotofthecanonicalvariatesarenot
shown).
Clonesfrom galsandpseudo-galswerethen
analysed(Fig.2).IntheplotofthefirsttwoCVs,whichtogetheraccountedfor72.3 % ofthetotal
variationofthedata(Table4), thescoresonCV1
andCV2 couldnotseparateclustersclearlybygalformationorfeedingsites, buttruegaldwelerson
leavesseparatedfrom pseudo-galdwelersonleaves
distinctlybyCV1, truegaldwelersonleavesandon
twigsoverlaps, anditisthesameastruegaldwelersontwigswithpseudo-galdwelersonleaves.
ThefinalCVAcomprisedaphidswithoutgals, a
plot(Fig.3)ofCV1 andCV2accountedfor69.5%and26.7% ofthetotalvariance, respectively(Table
4) provided evidentseparationsamong diferent
feedingsites, suchasleaves, barkofstem, twosites
containingtwigandculm, andthreesitescontainingleaves, petiolesandtwigs(Fig.3).
3.3　Clusteringanalysis
The clustering dendrogram showed the
separationsoffivegaldwelingaphidsbased onmorphologicalcharacters.Feedingsitesandgaltypes
ofthesefiveaphidsweremappedonthedendrogram
(Fig.4).TheresultindicatedthatthreePemphigusspecies, P.tibetensis, P.borealisandP.immunismade
thebasecluster, inwhichP.tibetensisandP.borealis
weremuchsimilaronselectedmorphologiesandthey
Fig.1.Plotofthemeanscoresonthefirsttwocanonical
variates(CVs)for122 fieldcloneswithdiferentgal
types, truegall(○), pseudogall(★)andwithoutgal
(■).
gottogetherfirst;thesethreePemphigusspeciesal
generatedtruegalonthetwigsoftheirhostplants.E.
imaicus, whichinducedpseudo-galsontheleaves,
joinedtothebaseclusterinsuccession.Another
Pemphigusspecies, P.matsumurai, showedarelativelylargephenotypic distance from the fourspecies
mentionedabove, itproducedtruegalsonleaves.
4　Discusion
4.1　Variationsofmorphologicalcharacters
The results indicated that diferent aphids
possesedmorphologicalvariations.TheCVvaluesofeverycharacterfordiferentaphidssuggested the
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ActaZootaxonomicaSinica动物分类学报 Vol.36　No.1
Fig.2.Plotofthemeanscoresonthefirsttwocanonical
variates(CVs)for74 galdwellingfieldcloneswith
diferentfeedingsitesandgaltypes, truegalonleaves
(△), pseudogalonleaves(■)andtruegalontwigs
(╋).
Fig.3.Plotofthemeanscoresonthefirsttwocanonical
variates(CVs)for48freelivingfieldcloneswithdiferent
feedingsites, leaves(△), barkofstem(╋), twosites
containingtwigandculm(★), andthreesitescontaining
leaves, petiolesandtwigs(■).
intraspeciesvariationsexist, becausethespecimens
werecolected from diferentplacesand during
diferentyears, thisresultwasthesameasthe
viewpointsofFootitandMackquer(1990), andSokal(1952).TheformersfoundthattheCVvalues
ofmorphologicalcharactersforCinaranigrainone
geographicalpopulationwere3.1 % -22.8 %;the
latercalculated theCV valuesofmorphological
charactersforPemphiguspopulitransversusamongdiferent
geographicalpopulations, therangewas3.1% -
16.3%.Themeansofaphidcharactermeasurements
werediferentamongspecieshere.Wecouldconclude
fromthedescriptivestatisticsthat, evensomeaphidspecieswereonthesamegenus, themeasurement
valuesandthemeansofsomecharacterswerestil
varied, suchasintwoChaitophorusspeciesandfour
Pemphigusspecies.
4.2 　 Morphologicaladaptationsofaphidstodiferentgaltypesandfeedingsites
TheresultoffirstCVArevealstheexistenceofdistinctmorphologicaldiferencesbetweengaldwelers
tofreelivingaphids.Themorphologicalseparationofthesetwoclustersdidnotinvolvetheexaminationof
singlecharacters, butwasbasedonCVA whichcompared the correlations between numerouscharacterswhichcloselycontactedwiththehostplant
surfaces.ThesecondCVAwasinordertoseparategaldwelingaphidclonesbydiferentgaltypesand
feedingsites.Theresultwasnotveryobvious, buttheseparationbetweentruegaldwelersfrompseudo-gal
dwelersboth on leaveswasdistinct. And thedendrogram ofgaldwelersshowedthediferencesamongdwelingondiferenthostplantsiteswith
respectivegaltypes.Furthermore, theresultoflastCVAseparatedfreelivingaphidclonesbydiferent
feedingsitesclearly.Theseselectedaphidsfedondiferentsitesofonegenushostplants, andpartsof
themcouldinducetoformgalsonhabitingsites, thesurfacestructuresofdiferentpartsdiferedfromeachother considerably. The CVAs based on the
morphologicalcharacterscontainingultimaterostralsegments, tarsalsegmentsⅠ , Ⅱ andclaws, which
wererelatedtofeedingandatachingonthesurfacesofhostplantsfordiferentaphids(Fangetal., 2006b).TheseparationsofdiferentCVAssuggested the
diferencesamongclustersofaphidswiththeselectedmorphologicalcharacters.Eachclusterwasrelatedwel
withdiferentfeedingsitesorgaltypes.Wededucedthataphidshadmorphologicaladaptationsbasedon
ultimaterostralsegments, tarsiandclawsvaryingwithdiferentsurfacetraitsoffeedingsitesandgaltypesonthehostplants.
Oneofthemajorevolutionaryhurdleswhichhadtobeovercomeforinsectstoliveonhostplantswas
theabilitytoremainatachingtothehostplants(Southwood, 1973), whichwasageneralabilityforphytophagousinsects.Insomeplants, surfacetextures
couldpreventaphidsfromholdingonthehostplants,suchasthesurfacesofpoplarsinthisresearch.Itwas
speculatedthatthesubstratesofdiferentsitesofPopulusdrivedthevariationsofsomeaphidmorphological
charactersforadaptingtotheindependentsurfaces;it
8
Jan.2011 方　燕等:蚜虫对杨属植物不同寄生部位的形态适应
Fig.4.DendrogramofclusteringanalysisbasedonMahalanobisdistancesamongfivespeciesofgaldwellers.The
leterinparenthesisdenotedthat(galtypes, feedingsites).P.Pseudogals.G.Truegalls.L.Onleaves.T.On
twigs.
canbeprovedbythediferentclustersondiferentCVAsandclusteringdendrogramcorespondingtogal
typesandfeedingsites(Figs1-4).
Theaphidswhichinduced toform galsorpseudo-galsonPopulusposesedrelativelyshorter
ultimaterostralsegmentsthanotherspecieswhich
couldnotinducegals(Table3).Theleafgal
dweler, P. matsumurai, possessed longerultimaterostralsegmentsandtarsithantwiggaldwelers, P.
immunis, P.tibetensis, andP.borealis, andleafpseudo-
galdweler, E.imaicus(Fig.4;Table3).Galsare
the extended phenotype ofaphids (Stone andSchönrogge, 2003).Aphidsarephloemfeedersand
divertplantasimilatesto gals, thereby actas
nutrients.Galingsuccessresultedfrommakingthegalasastrongersink(Wool, 2004).Aphidscanacquire
nutrientseasilyfrom gals, sorelativeshortultimate
rostralsegmentwas suficientenough for their
survival.Basedonnutritionhypothesis(StoneandSchönrogge, 2003)andtheevolutionarytendencyof
gallocationsinEriosomatinae(ZhangandQiao,
2007a;2007b), thegalsontwigscaninterceptmore
nutrientsthanothersonleaves, sotheaphidsinducinggalsonleavesdevelopedlongultimaterostralsegments
inordertogetingmuchalimentation.Amongfree
livingaphids, multi-sitelivers, C.populetiandPt.
neimogolense, havelongertarsiandclawsthanleaflivers, C.populialbaeandD.populi, andbarkliver,
Ph.paserini(Table3).Wepresumedthataphids
feedingonmulti-sitesneedmorecreepingabilitythanfeedingononesite, becausetheyneedreachmany
feedingsites.Moreover, theaphidsfeedingonbarks
ofstemshave relatively longer ultimate rostral
segmentsandshortertarsalsegmentthanthatfeedingonleaves(Table3).Thesurfaceofstem barksis
rougherthanleaves, andthefeedingplacesofaphids
onstembarksaremuchdeeperthanonleaves.Sothebarkliverrequiredlongultimaterostralsegmentsfor
feedingandshorttarsalsegmentforatachingbeteron
roughsurface, itwassustainedbythatM.schreiberionthesmoothsurfacesofQuercusilexleavesheldonfar
beterthandidT.annulatus, becausetheformerhad
longertarsithanthelater(Kennedy, 1986).Italso
canbededucedfromourstudythattherostrumlengthwascorrelatedwiththeaphidsfeedingsites(Bradley,
1959;1961).Inaword, aphidspecieswithdiferent
galtypesandfeedingsiteshavediferentstatesof
morphologicalcharacters, whicharerelatedwithaphidfeedingandtouchingonthesurfacesofhostplants.
The122 aphidfieldclonesbelongtotenspecies
weredividedintodiverseclusterscorespondingtodiferentfeedingsitesandgaltypes.Theaphidsfor
eachfeedingsitesandgaltypesshowedrespectively
diferentmorphologicalcharactervariations.Every
feedingsiteorgaltypewastightlyrelated withdiferentsurfaceofhostplants, foreitherthegalinner
surfaceortheappearancecharactersofhostplants.
Theseindicatedmorphologicaladaptationofaphidsto
hostplants.Twentyyearsago, morphologicaladaptationto
hostshadnotbeenreceivedatentionasaposible
complicationinreconstructingherbivorephylogenies
anddeterminingtheirrelationshipstohostphylogenies(MiterandBrooks, 1983).Butnow, whenthe
phylogeneticrelationshipwasanalyzedandtraditional
taxonomywasdoneaboutphytophagousinsectbymorphologicalcharacters, morphologicaladaptation
shouldbeconsideredsuficiently.Itwasrevealedfrom
thestudythataphidswithdiferentfeedingsitesonthe
samegenushostplantsweremorphologicalyadaptedtodiferentgaltypesandfeedingsitesonhostplants,
although theseaphidsliein diferentgenera or
9
ActaZootaxonomicaSinica动物分类学报 Vol.36　No.1
subfamilies.Basedonabovestudy, wefoundthatal
investigationswerenotcarriedwithuniquecharacter.
Thus, combinedmorphologicalcharactersarethemostusefultomorphologicalresearch.Morphologywas
tightlyassociatedwithbehavior, ecologyandother
related aspects. So, studying on adaptationsofphytophagousinsects to their hostplants must
particularlytakeaccountoftheseaspects, whichmight
influencetheadaptation.
Acknowledgements　WearegratefultoTIANShi-
Bo, ZHONG Tie-Sen, WANG Sui-Ying, MENGGuang-Xiang, ZHANG Bao-Lin, YU Zhi-Shou,
ZHENG Fa-Ke, MAO Jin-Long, HE Fu-Gang,
WANG Fu-Lin, DUANZhen, CHEN Wei-Dong,WANG Lin-Yao, HU Xin-Zhen, WANG Ze-Fen,
SONG Shi-Mei, YANG Han-Yuan, HUANG Fu-
Sheng, WANG Yong-Xian, WANG Zi-Qing, LIUJin-Rui, HETong-Li, ZHANG Dong, LIU Hong,
LIJing-Huaforcolectingthespecimens.Wethank
YUANDe-ChengandZHANGHe-Caiforreading
and commenting on the earlier version ofthismanuscript, andtoLIU Cai-PingoftheInstituteof
Zoology, ChineseAcademyofSciencesformaking
slides.
REFERENCES
Albrecht, G.H.1980.Multivariateanalysisandthestudyofform,
withspecialreferencetoCanonicalVariateAnalysis.Am.Zol., 20:
679-693.
Bernays, E.A. 1991.Evolutionofinsectmorphologyinrelationto
plants.Philos.T.R.Soc.B., 333:257-264.
Blackman, R.L.andEastop, V.F.1994.AphidsontheWorlds
trees.Anidentificationandinformationguide.CABInternational,
Walingford, UK.1-986.
Blackman, R.L.andEastop, V.F.2000.AphidsontheWorlds
crops.Anidentificationandinformationguide, secondedition.
TheNaturalHistoryMuseum, London, UK.1-466.
Bradley, G.A.1959.FeedingsitesofaphidsofthegenusCinaraCrutis
(Homoptera:Aphididae)inNorthwesternOntario.Can.Entomol.,
91:670-671.
Bradley, G.A.1961.Astudyofthesystematicsandbiologyofaphids
ofthegenusCinaraCurtisinCanada.Ph.D.thesis, McGil
University, Montreal, Canada.
Fang, Y, Qiao, G-XandZhang, G-X 2006a.Diversityofhostplants
andfeedingsitesofaphids.ActaZootaxonomicaSinica, 31 (1):31-
39.[动物分类学报 ]
Fang, Y, Qiao, G-XandZhang, G-X 2006b.Morphometricvariation
ofeightaphidspeciesfeedingontheleavesofbamboos.Acta
Entomol.Sin., 49 (6):991-1 001.
Foottit, R.G.andMackquer, M. 1980.Morphometricvariation
betweenpopulationsofthebalsam woolyaphid, Adelgespiceae
(Ratzeburg)(Homoptera:Adelgidae), inNorthAmerica.Can.
J.Zool., 68:1494-1 503.
Footit, R.G.andMackquer, M. 1990.Morphometricvariation
withinandbetweenpopulationsofthepineaphid, Cinaranigra
(Wilsom)(Homoptera:Aphidoidea:Lachnidae), inWestern
NorthAmerica.Can.J.Zol., 68:1 410-1 419.
Ilharco, F.A.andvanHarten, A.1987.Systematics.In:Minks, A.
K.andHarrewijn, P.(eds.), Aphids, TheirBiology, Natural
EnemiesandControl.Vol.A.Amsterdam.Elsevier, Holand.
pp.51-77.
Kennedy, C.E.J.1986.Attachmentmaybeabasisforspecialization
inoakaphids.Ecol.Entomol., 11:291-300.
Li, G-H 1984.Botany.ShanghaiScientificandTechnicalPublishers,
Shanghai.1-417.
Ma, Q-Y2003.Thenameconfluenceofthefernandtheangiospermin
China.QingdaoPress, Qingdao.1-1 561.
Miter, C. and Brooks, D. R. 1983.Phylogeneticaspectsof
coevolution.In:Futuyma, D.J.andSlatkin, M. (eds.),
Coevolution.Sinauer, Sunderland, UK.pp.65-98.
Moran, N.A. 1986.Morphologicaladaptationtohostplantsin
Uroleucon(Homoptera:Aphididae).Evolution, 40 (5):1 044-
1 050.
Peeters, P.J.2002.Correlationsbetweenleafstructuraltraitsandthe
densitiesofherbivorousinsectguilds.Biol.J.Linn.Soc., 77:43-
65.
Qin, J-D 1987.Relationshipofinsectsandplants.SciencePress,
Beijing.1-227.
Remaudière, G.andRemaudière, M.1997.CatalogueoftheWorlds
Aphididae.InstitutNationaldelaRecherché Agronomique, Paris,
France.1-473.
Reyment, R.A., Blackith, R.E.andCampbel, N.A. 1984.
Multivariate Morphometrics, 2nd Edition. Academic Press,
London, UK.1-233.
Sokal, R.R. 1952.VariationinalocalpopulationofPemphigus.
Evolution, 6:296-315.
Southwood, T. R. E. 1973. The insect-plantrelationship-an
evolutionaryperspective.Symp.R.Entomol.Soc.Lon., 6: 143
-155.
Stone, G.N.andSchönrogge, K.2003.Theadaptivesignificanceof
insectgalmorphology.TrendsEcol.Evol., 18:512-522.
Wool, D.2004.Galingaphids:specialization, biologicalcomplexity,
andvariation.Annu.Rev.Entomol., 49:175-192.
Zhang, H-C andQiao, G-X 2007a.MolecularphylogenyofFordini
(Hemiptera:Aphididae:Pemphiginae)inferredfromnucleargene
EF-1αandmitochondrialgeneCOⅠ .B.Entomol.Res., 97 (4):
379-386.
Zhang, H-C, andQiao, G-X 2007b.Systematicstatusofthegenus
FormosaphisTakahashiandtheevolutionofgalsbasedonthe
molecularphylogenyofPemphigini(Hemiptera:Aphididae:
Eriosomatinae).Syst.Entomol., 32 (4):690-699.
Zhang, G-X, Qiao, G-X, Zhong, T-SandZhang, W-Y1999.Fauna
Sinica, Insecta, Vol. 14. Homoptera: Mindaridae and
Pemphigidae.SciencePress, Beijing.1-356.
Zhang, G-XandZhong, T-S1983.EconomicInsectFaunaofChina.
Fasc.25.Homoptera:Aphidinae, part1.SciencePress, Beijing.1
-387.
10
Jan.2011 方　燕等:蚜虫对杨属植物不同寄生部位的形态适应
＊通讯作者 , E-mail:qiaogx@ioz.ac.cn
蚜虫对杨属植物不同寄生部位的形态适应
方　燕 1, 2　黄晓磊 1　乔格侠 1＊　张广学 1
1.中国科学院动物研究所 , 动物进化与系统学重点实验室　北京　 100101
2.华东师范大学生命科学学院　上海　 200062
摘　要　为了明确取食相同植物不同部位和营不同虫瘿的蚜
虫是否存在形态适应 , 论文以取食杨属 Populus植物的 10种
蚜虫为研究对象 , 基于蚜虫喙末端 、 各足跗节和爪的形态测
量数据 , 对 122个克隆的形态变异通过一般的统计描述 、 典
型变量分析 (canonicalvariatesanalysis, CVA)以及聚类分
析等方法进行了研究 。结果显示 , 不同的蚜虫克隆间形态特
征存在分异 , 与不同的虫瘿类型和取食部位相关。 3个典型
变量分析明显地区分了形成虫瘿和不形成虫瘿的蚜虫克隆 ,
在叶片上形成真虫瘿和伪虫瘿的克隆以及不产生虫瘿的克
隆 , 并形成明显的克隆簇。而用于分析的形态学特征 , 如喙
末端 、 跗节和爪的测量值 , 其一般统计描述的差异也支持这
些区分。蚜虫自然种群不同克隆簇的区分很好地对应了不同
的取食部位和不同的虫瘿类型 , 且各簇的形态特征体现了各
自的特点 , 表明了蚜虫对杨属植物已经形成了良好的形态适
应。同时 , 也初步讨论了不同蚜虫克隆簇形态适应产生的原
因。并建议在基于形态特征探讨昆虫的系统发育关系和进行
传统分类时 , 必须考虑昆虫形态特征的适应性;在深入研究
昆虫与寄主植物相互之间关系时 , 需要将各种形态特征综合
考虑并关注其它的影响因素。
关键词　蚜虫 , 取食位点 , 虫瘿类型 , 形态适应 , 杨属.
中图分类号　Q969.3
11