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Origin and Evolution of the Apotomopterus Ground Beetles (Coleoptera, Carabidae) as Deduced from Mitochondrial ND5 Gene Sequences PDF

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Preview Origin and Evolution of the Apotomopterus Ground Beetles (Coleoptera, Carabidae) as Deduced from Mitochondrial ND5 Gene Sequences

Elyt・,a,「olive,27(2):643-649,November13,1999 OriginandEvolutionoftheApotomopterusGroundBeetles (Coleoptera,Carabidae)asDeducedfromMitochondrial ND5GeneSequences Cheong-GenKIM,Zhi-HuiSU,YukiIMURAl)andSyozoOsAwA JTBiohistoryResearchHall,1-1Murasaki-Cho,Takatsuki,Osaka,569-1125Japan,and 1)DepartmentofGynecology,TokyuGeneralHospital,Kita-senzoku1-45-6, Ota-ku,Tokyo,145-0062Japan Abstract Phylogenetic trees have been constructed from the mitochondrial NADHdehydrogenasesubunit5(ND5)genesequencesof13species(27specimens)of Ca,abus(Apoto,,1opte1-11s)withC.(Llnlnoca,・abus)clat11,atusandC.(L),naackiasout- group.TheND5 treesindicatethat thereare threemainlineages. 0neofthespecies,C. (A)sauteri,ismorphologicallydividedintoseveralsubspeciesbyslightdiffeirences.Seven specimensoffoursatlte,-1subspeciesfromvariouslocalitiesinmainlandChinaandTaiwan havebeenclassifiedbytheND5genesequencesintothreecladeswiththeirancientsepara- tionca 22MYA.Ca,abus(A)1/upeensls,whichshowsconsiderablemorphologicaldiffer- encefromC.(A)saute1・i,branchedofffromoneofthesa1lteristems. Introduction ThesubgenusApotomopterusofthegenusCa,・abus(s lat)comprisesnearly100 speciesdistributedinChinaandtheadjacentregionsincludingTaiwan. Intheprevious paper(IMURAeta1., l998),aphylogenetictreeoftheNADHdehydrogenasesubunit5 (ND5)genesequencesfrom9taxaofthesubgenusApotomopteruswasreported. In thepresentstudy,revisedphylogenetictreeshavebeenconstructedbyadding10taxa, usingtwo umnocarabussequencesasoutgroup.Basedonthetrees,evolutionaryhis- toryanddiversificationpatternwithinthesubgenusApotomopterusarediscussed. Materials and Methods Thespeciesanalysed for theND5genesequences including thepreviously re- portedones(IMURAeta1.,1998)arelistedinTable t.Fortheanalyticalmethodsand constructionofthephylogenetictrees,seeSUetal. (1996,1998)andKIM,ZHoUetal. (1999).Usingtheneighbor-joining(NJ)method(SAITou&NEI,1987)andunweighted pair-groupmethodwitharithmeticmean(UPGMA)(KUMAReta1.,1993),thephyloge- netictreeswereconstructedusingthesequencescontainingale69bp3'-regionofthe ND5geneof19taxaof thesubgenusApotomopterus. Bootstrapanalysiswasper- formedforthetreesbasedon500resamplings(FELsENsTEIN, l985).Theevolutionary 644 Cheong-GenKIMofaf .一一一し ,s)‘s一一S加 ' 加erycs,:.“ 2.一一ee-S・ s・〇fly,t- 1 -一一s)一一 'M 加M e,・s3 jCC一「一一as))),M.,==一a“ 'M.'Esp yy60s“,--,M・一一 ・45s“ 7 Lineage1(●サ C )sa - 'lcs“ 81一0 C )sa ・ 'nIi C )sa ・ 'r t2 C ) 'M前 u - C s) .s 14 C s)ro .s 15 CC s))a“ m, p・-e‘al7a-s16 L.meage2 C ) ,o ngm ao9en918 C .)to - ,2o C ) =.-:=・ sp2l - C s) 在ao 22 CC .)a「 。 ・ m or一一.oha「,-・24一一S23 L.mea 3 ■ C ):!r 25 C )c s“ m 26 C ) P 27 C .mno ,、・一al n‘s C )ma 一一商.s 0.06 Distance MYA distances(D)werecomputedbyKIMURAs' two-parametermethod(KIMURA, l980).For settingthetimescale,a0.01Dunitcorrespondingto3.6millionyears(MYR)was used(SUeta1.,1999). ResultsandDiscussion OriginandPhylogeny. ApotomopterusisthesolesubgenusinthedivisionSpinulatiofthegrandgenus Carabus,anditsmembersconstituteawell-definedmonophyleticclusterontheND5 phylogenetictrees(IMURAeta1., l998).Thepresentphylogenetictreesindicatethat therearethreemainlineagesoftheApotomopterusspeciesthathavebeenexamined (Fig. l).ThefirstlineageincludesC.(A)kouich1i fromNorthVietnam,C.(A)sauteri' andC.(A)hupeensisfromtheChineseContinentandTaiwan.Carabus(A) kouichii andC.(A)sauteriseparatedlongtimeago[ca32millionyearsago(MYA)].Follow- ingthis,threeC.(4.)sauterisublineagesdivergedataboutthesametimeca22MYA. OneofthemcontainingC. (4.)s dayaoshanlcusandC.(,4.)s.ssp also includes five specimensofC.(A)hupeensls,indicatingthatC.(4.)hupeensisfromvariouslocali- tiesbranched off fromoneofthesauteristems. Thesecond lineagecontainsC. (4.) tonkinenstsfromNorth VietnamandC. (A) toulgoeti,C. (‘4.) delavay1,andC. (A) tuxeni from Central and South China. Carabus (‘4.) toulgoet1 and C. (A) ton- kinensls/C.(A)tux:enl/C.(A)delavayiseparatedca25MYA, followedbydiversifi- EvolutionofApotomopte''fisGroundBeetles 645 Lineage1ォ●) ] u・nea9e2 ▲) l unea9e3 ●) D:0.01 cationofthelatterthreespeciesca. l4MYA.ThethirdlineageconsistsofC.(4.)cler- montianusfromNorthVietnam,andC.(A)cyanlpennlsssp.,C.(A) iris,C.(A)sp. (alliedtoC breunlngianus; IMURAeta1.,1999),C.(A)art・owl,C. (A) laoshantcus 1iaorumandC.(A)1. laoshamcusfromCentralandSouthChina.Carabus(A)cler- montianusandC. (A)sp.separated fromacommonancestorca26MYA,andthere- mainingspecies diverged ca. 18 MYA into two sublineages, i.e., C. (A) cyan1- ds)/ . . pemzs/C.( ) faosヘamcMsffaorum C (4. aos ンamcu an C )arrowl/C.( .) iris.Furtherdiversificationintothreeandtwodescendantspeciestookplacewithinthe respectivesublineageslessthan5MYA. TheoriginofApotomopterusisoldandcanbetracedbacktothetimeoftheex- plosiveradiationof theCarabina50-40MYA(seeSuet al., 1999).Thus, Apoto- mopterus may beconsideredasone of thegroupsoriginatedupon the radiation. Shortlyaftertheradiation,threelineagesshowninFig.1anddiscussedabovediverged almostsimultaneouslypresumablysomewhereinthesoutheasternregionoftheChi- Fig.1(onpp.61'1 645). PhylogenetictreesofthemitochondrialND5gene(1,069bpupstreamfrom3' terminalstopcodon)fromtheApoto'nopterusspecies.TheUPGMAtree(A)andtheNJtree(B).The bootstrapconfidencelevel(%)(basedon500resampIings)isshownateachbranchingpoint.Distance (D)denotesKIMURA'stwo-parameterevolutionarydistance(KIMURA,1980).Thesequencesofthe specimens8-10,andthoseof19and20wereidentical,respectively. 646 Cheong-GenKIMelal Fjg 2 MapshowjngthecollectingsitesoftheApoto,1lopte'u'sspeciesusedinthisstudy.Nume「alS correspondIothoseshowninTabletandFig.1.●,lineage1;▲,lineage2;■,linea9e3. noseContinent(seefig.32ofIMuRAeta1., l998).Figure2andtheND5treesindicate thatthedjstributionrangesofthethreelineagesarewideandoverlapconSide「ably.No definitedistributionboundariesbetween themcanbedrawn, Thissuggeststhat the Apotomopterus ancestor was divided into at least three isolates upon gee9raPhiC changesofthecontinentca37MYA.Theneachisolateexpandeditsdistributionto occupythepresenthabitat. Patter morp ofogz'ca evoftefzon Foursauterisubspecies,dayaoshanicus,yunkaicus,sauteriandssp.(population fromMt.JinggangShan)differonlyslightlyfromoneanother,eventhoughtheyhave beenclassifiedassubspecieswithinthesamespecies(IMuRA, l994,1995&1999). However,theirseparationoccurredlongtimeago,ca22MYA(Fig.1).Carabus(A) clermontjanusandC.(A)sp arealsosimilar inmorphology,buttheyshowaremote phylogeneticrelationship,separatedca26MYA.Thus,evenifmorethantwotaxaa「e treatedasthesameoralliedspeciesbecauseofsimilarmorphology,their timeofdi- EvolutionofApotomopte,・usGroundBeetles 647 u一一 一一 EI ' u O a N e,、 ,n 、o r、 co o、 c e - t、、l ,,、 、r、、o t、 ∞ o、 o - ・f、 ,.n、o l、 〇 00 00 00 00 00 00 00 0、 0、 0、 0、 0、 0、 0、 0、 0、 0、 0、 0 0 0 0 0 0 0 0 00 / u l- 、r、'''、 、・r、'・n 、・r、、n -aa o-s 9_ 9_ 9_ 9_ 9_ 9_ 9_ 9_ 9一 9一 9_ 9一 9一 9_ 9_ 9一 9ー 9一 9_ 9一 9一 9_ 9一 8_ 9一 9一 l'・1 ;W s3 m oo m m l:o l:o ,:o f:1;l l:o l:o l:,:I l:o m l:l:1 l:o o /,r国 oV ・,:'l: <l: <l:<( <l: <l: <l: <l: ao (I (] al-一 u-- 〇 ;>Pn、 ,x一 -x cL)--ss-juPa)snsuou1-oa)dss:n:一-doo-oミ :>Ieee、一一、一 -I--Jxumisnsug-x3uo一一一一) m-fxumfS'Sue-X3ueA'N〇一W--o-oqnHnuouuofs- eu-urn--S'N'一〇国s-o-uejS3u eu--um-S'aNuSnM3um'-〇一〇 W--,x3ue-nSuS3ug33u-f'-〇一「 m-x3um'Sa'-一〇一〇〇u jSe-」〇〇3um'Nu'-,3u-d3ue-uV〇国 -um'9N,uSo.o'-3uunuoH〇」一一 ueielnN,niu--s・ uejueNueM-elno-ueN・ oee-d'-〇Euo-A'N'odaoeサ一一」〇u Euo->'N,'Aod-eoe-uolMe-ooa一一」〇」 ueu-oN->od-eo-'uolu--ooaサ一・」〇 u-ueuunA's-eqeH一・ u-一urn--S'SuenfueA,3ue-X一mfoumfo-ss,s-ea一・・一一ueis3u m--x3um'Nu〇一〇Sooe-」'- u-furn--S'NuefSnum'-〇一国〇 u-一-x3um'aNugjSooe-〇」'- ea・一eu---xumuefSo〇一〇・国 Snoe-m--x3um'N'u〇一〇'- m--oum--sss-・・s3uega一一uMW-o'N-Aodnidサ一」u-AoeaMei'- -ou--no--z-nSue-Xoq--〇〇・国u sope-Nn」ugMo'Nuosj」〇 No-esuedef'N,oMoV一」 JIo -s 'I一、 (9 6 olq :>coo、一一一 'ON *ト 0*0 0、 =* - - 一 ー ート 0一0 0*0、 一 * * t ト 6-)o・ e l;- - l n s u,o u」 .1:i * :- ・ ・1 ミ ,j ミ- ,i 'S (866 scods、一一 一- ._ 美・ ・ 美・0 美・0 ・ ・ ・一 ・一 . . . o- ・ - ・ .'ミ= ・= -・'ei ・o -)'-o-v: . ・ :, o :)二 : - i; -、: -、: -、: -'、: -'、: '-:、 -':' -':、 -':、 -:、 -': -1、 -'、:一、 M .:-1: -S-: 、一:'、一1、一' - 、一1 :、一: - 、一・ 、一' 、一1 o」 0 (_) _1 648 Cheong-GenKIMetal vergenceisnotnecessarilyrecent.Sucha“silentmorphologicalevolution”canberec- ognizedinothercarabidssuchasDamasterblaptoides,Phricocarabusglabratus,To(- mocarabusspp.,etc.(SUetal.,1999). Asnotedabove,C.(4.)hupeensissplit fromoneoftheC.(A)sauteristemsin- cludingC.(A)sdayaoshanlcusandC.(A)s.ssp.ThissuggeststhatC.、(A)hupeen- sisemergedwithaconsiderablemorphologicalchange fromC. (A)sauteri whose morphologyhasremainedalmostunchanged foralong time.Thespeciationofthis typeresemblesthebranchingofC.(Euleptocarabus)porrectico11is fromtheC. (Lim- nocarabus)clathratusstem(IMURAeta1.,1998;KIM,SUeta1.,1999;SUeta1.,1999). Thedifferenceinmorphology betweenC.、(A)cyanlpennisandC. (A) laoshanlcus, andbetweenC.(A)arrowiandC.(A) irisareconsiderable,andyettheirdiversifica- tionoccurredrecently.Thus,evolutionofApotomopterushasbeenbroughtaboutby havinga silent phaseandaphaseaccompaniedby a considerablemorphological change,ashasbeenwidelyrecognizedintheothercarabidgroups(Suetal.,1999) Acknowledgements Wearegrateful tothe followingcolleagueswhokindlysuppliedwithvaluable specimens for thepresentstudy:Prof ]) CAwAzzUTl (Pagno, Italy), Dr. S.MURzIN (Moskow),Dr.ShuheiNoMURA(NationalScienceMuseum,Tokyo),Mr.A.SHAMAEv (Moskow),Mr.J.TuRNA(Czech)andDr.H.-Z.ZHou(AcademiaSinica,Beijing).This study issupportedinpartbytheGrant-in-aidNo.09041167forOverseasResearchof theInternationalScientificResearchProgramfromtheMinistryofEducation,Science, Sports andCulture, Japan, to the fieldwork in Vietnamby Dr.Shuhei NoMuRA. ThanksarealsoduetoHidekoTANAKA forskillful technicalassistance. 要 約 金 衝;坤・蘇 智慧・井村有希・大澤省三: ミトコンドリアND5造伝子によるトゲオサムシ IIE属(Apoto″1opterus)の系統解析. - Apoto,;,opterusは, 雄の交尾器内袋基部に基棘と呼ばれる 硬化片を持つトゲオサムシ群の唯一の構成貝で, 中国南東部を中心に分布し, 100種近くを含 む大亜属である. 本研究では, IMuRAら(l998)の報告に加え, 中国とその周辺地域からえられ たトゲオサムシ亜属19分類単位 (27個体) のミトコンドリアND5遺伝子の塩基配列から系統 関係を検討した結果, 3系統の存在が認められた. これらの3系続は, オサムシの一斉放散 (約5~4千万年前) 直後にほぼ同時に分岐し, さらに各系統の中で2~3回にわたって分岐が起 きたと推定された. Ca,abus(11りotomopte,・us)saute,iは, 中国南東部と台湾にぃくっかの亜種を 産するが, 形態的にはたがいによく似てぃるため, その分化は比較的最近に起つたものと想像 されがちである. しかし, mtDNAの結果ではsaute,・iは3つの系統に分かれ, それぞれ2200万年 前の古い時代に分岐したことが示唆された. また, c (d)sp. (ブロイニングトゲオサムシに近 縁な未記載種) とC.(A)clermontianusも基本形態はたがいによく似ているが, mtDNAから両者 は非常に古い時代に分化していることが示された. 一方, C.(A)sauteriの一つの枝からC.(A) EvolutionofApotomopte,-ttsGroundBeetles 649 hupeensisが分岐しているが, この事実は, 長いあいだ形態変化がほとんどなかったsauteriから, 形態的に異なる種が出現したことを示唆している. さらに, C. (A)cyampennisとC.(A) 1aoshanicus,およびC.(A)a,,-owiとC.(A),risとのあいだでは, 顕著な形態的差異にもかかわら ず, 分子系統樹からみるとそれぞれの種の分岐した時期は比較的新しいことが判明した. 以上 の結果から, トゲオサムシ亜属の進化には, 形態が長いあいだほとんど変わらなかった時期と, 短いあいだに変化した時期のあることが示唆された. References FELsENsTAIN,J.,1985. Confidencelimitsonphylogenies:Anapproachusingthebootstrap. Evolution, 39:783-791. IMuRA, Y.,1994. Apreliminary revisionof thespecies-complexofCa,abus(Apotomopterus)sauteri (Coleoptera,Carabidae). Elyt・,a,To(kyo,22:1-14. - 1995. NotesontwoApoto,nopterusspecies (Coleoptera,Carabidae) from northern Vietnam. Bull natn.Sci.Mus.,「okyo,(A),21:l-5. - &K.M1zUsAwA,1996. TheCa,abusoftheWorld.InFUJITA,H.(ed),Mushi-Shaslconographi- ca1SeriesofInsects,2.261pp.,84pls.Mushi-sha,Tokyo.(InJapanese,withEnglishbooktitleand summary) - ,C.-G.KIM,Z.-H.Su &S. 0sAwA,1998. AnattemptatthehigherclassificationoftheCarabina (Coleoptera,Carabidae)basedonmorphologyandmolecularphylogeny,withspecial reference to Apotomopte,-us,Lim,toea,abusandEuleptoca,・abus. Elyt,・a,「okyo,26:17-35. H.-Z. ZHou & Z.-H.Su,1999. AnewspeciesofApoto"1opte,-usandanewsubspeciesofCy- - , chrus(CoIeoptera,Carabidae)fromChina. Ibid.,27:651-654. KIM,C.-G.,Z.-H.SU,0.ToMrNAGA&S.0sAwA,1999. OriginanddiversificationofEuleptocalabuspor- rectico11is(Coleoptera,Carabidae)intheJapaneseIslandsinferredfrommitochondrialND5genese- quences. Met.Phy1ogenet.Eyot.(inpress). - ,H.-Z.ZHoU,Y. IMURA,0.ToMINAGA,Z.-H.SU&S.0SAWA,1999. Patternofmorphologicaldi- versificationintheLeptocalabusgroundbeetles(Coleoptera,Carabidae)asdeducedfrommitochon- drialND5geneandnuclear28SrDNAsequences. Met.Biol.Eyot.(inpress). KIMURA,M.,1980. Asimplemethodforestimatingevolutionaryrateofbasesubstitutionsthroughcom- parativestudiesofnucleotidesequences. J.,not.Eyot.,16:111-120. KUMARS.,K.TAMURA & M.NEI, l993. MEGA(MolecularEvolutionaryGeneticsAnalysis),version 1.01.ThePennsylvaniaStateUniversity,UniversityPark,PA. SAITou,N.,&M.NEI,1987. Theneighbor-joiningmethod:anewmethodforreconstructingphylogenetic trees. Met.Biol.Eyot.,4:406-425. SU,Z.-H.,T.0HAMA,T.S.0KADA,K.NAKAMURA,R.ISHIKAWA&S.0SAWA,1996. Phylogeneticrelation- shipsandevolutionoftheJapaneseCarabinaegroundbeetlesbasedonmitochondrialND5genese- quences. Jmet.Eyot.,42:124-l29. - , 0. ToMINAGA, M. 0KAMoTo& S. 0sAwA, l998. Originanddiversificationofhindwingless Da,naste,・groundbeetleswithintheJapaneseIslandsasdeducedfrommitochondrial ND5genese- quences(Coleoptera,Carabidae). Met.Biol.Eyot.,15:1026-1039. C.-G.KIM,Y. IMURA, 0.ToMINAGA,M. 0KAMOT0&S. 0SAWA, l999. DiscontinuousevOlution - , of thecarabidgroundbeetles(Coleoptera,Carabidae) inferredfrommolecular phylogenetictrees. (Submitted).

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