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What Is the Relationship Within the Family Lamnidae?

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What Is the Relationship Within the Family Lamnidae? TurkJBiol 31(2007)109-113 ©TÜB‹TAK WhatistheRelationshipwithintheFamilyLamnidae? MineDOSAYAKBULUT DepartmentofMedicalBiologyandGenetics,FacultyofVeterinaryMedicine, AfyonkarahisarKocatepeUniversity,Afyonkarahisar-TURKEY Received:01.06.2006 Abstract: UncertaintiesremainabouttherelationshipwithinthefamilyLamnidae,whichincludesthewhiteshark,2makos,the porbeagle,andsalmonshark.SeveralalternativehypotheseshavebeensuggestedrelatedtotheLamnidaephylogeny.Theaimof thisstudywastofindanaccurateanswertothefamilyLamnidaeinterrelationship.Tothatextend,themitochondrialcytochrom eb genewasstudiedinalltheLamnidaespeciesand2outgroupsfromthefamiliesAlopiidaeandOdontaspididae.Themonophylyof2 makoswereobtainedfrombothDNAandaminoacid(AA)parsimonyanalysis.Basedonouranalysis,firstthewhitesharkjoinsthis group,whichisasistertaxontothegenus Isurus (makos),asreportedbyNaylor.IntheAAparsimonyanalysis,the2makosand porbeagle-whitesharkbranchescometogetherasthemonophyleticfamilyIsurus,butnotLamna.Theseresultsagreewith Compagno’ssuggestionandMartin’sfindings. KeyWords: Lamnidae,phylegenetic,relationship LamnidaeFamilyasi‹çindeki‹liflki Özet: Beyazköpekbal›¤›,2mako,porbeagleveSalmontürüköpekbal›klar›n›kapsayanLamnidaefamilyas›içerisindekiiliflkiçoknet de¤ildir.Bufamilyan›nkendiiçerisindekis›n›fland›rmas›nayönelikpekçokfarkl›hipotezlerüretilmifltir.Buçal›flma,Lamnida e familyas›içindekiiliflkilereyönelikyeterlibircevapbulabilmekamac›iletümLamnidaetürleriniveAlopidaeveOdontaspidid ae ailesinden2hariciörnekkullan›larakmitokondrialcytbgeniileyap›lm›flt›r.HemDNAhemdeAAprsimonyanalizlerinde2makotürü monofiletikgrubolarakeldeedilmifltir.BugrubaNaylor’›nsonucunauygunolarak,1analizdemakolar›nba¤l›oldu¤uIsuruscins inin kardeflcinsiolanbeyazköpekbal›¤›kat›l›rken,AAanalizisonucundaporbeagle-beyazköpekbal›¤›ile2makocinsibiraradag rub oluflturmakta.IsuruslarbuanalizdemonofiltretikgrubhalindeikenLamnacinsimonofiltretikde¤ildir.BusonuçCompagno’nun önerisiveMartin’inbulufluileayn›d›r. AnahtarSözcükler: Lamnidae,genetics›n›fland›rma,iliflki Introduction asfastswimmingsharks;sometimescalledthelamnid, Evolutionaryrelationshipswithinandbetween isurids,ormackerelsharks.Theirbodieshaveadaptedto differentordersofsharkshavebeendiscussedby high-speedswimming,forwhichtheyhaveaconical taxonomistsforalongtime.IntheorderLamniformes snout,verylargegillsformoreefficientgasexchange,a (mackerelsharks)thereare7families:Lamnidae streamlinedfusiformbody,averysmallseconddorsalfin, (mackerelsharks),Alopidae(threshershark), andastronglunatetail.Someofthesesharkscan Odontaspididae(sandtigershark),Cetorhinidae(basking maintainabodytemperature7-10°Chigherthanthe shark),Megachasmidae(megamouthsharks), watertemperaturebyexchangingheatthroughthe Mitsukurinidae(goblinsharks),andPseudocarchariidae circulatorysystem,whichkeepsheatinsidethebody(3). (crocodileshark)(1). Theyaremostlyseenincoastalwaters,incooltotropical seas(1). TheLamnidaeisaverysmallfamilyandincludesonly 5species,includingthewell-knownpredatorsthewhite Manyresearchershavetriedtobetterunderstandthe shark,2makos,theporbeagle,andsalmonshark(2). elasmobranchphylogenyandtherelationshipbetween Mostly,theyhaveaverylargebodysizeandareknown thedifferentorders.First,Compagno(4,5)presenteda 109 WhatistheRelationshipwithintheFamilyLamnidae? newclassificationmodelinwhichhegroupedthe Inanalternativehypothesis,LongandWaggoner elasmobranchordersinto4superorders:Galeomorphii, proposedthatCarcharodonandLamnaaresistertaxa, Squatinimorphii,Squalomorphii,andBatoidea.He basedonanalysisoftoothcharacters(8,9). assignedCarcharhiniformes,Lamniformes,and Athirdalternativehypothesiswasproposedby OrectolobiformesintothesuperorderGaleomorphii.He Maisey,basedonsimilarmorphologicalcharacters.This consistentlydefendedthemonophylyofeachgaleomorph propositionincluded14speciesofLamniformes.The order,particularlyhissuggestionaboutthemonophylyof authorsuggestedthatthefamiliesLamnidaeandAlopidae theLamniformes(4),basedondentitionandmanyother aremonophyleticandthesistergroups,Cetorhinusand anatomicalformations.Lamnoidsharksaregenerally Megachasma,jointhisgroupfirst(10,11). consideredcloselyrelatedtocarcharhinoidsharksbecause oftheirsimilaritiesinfinpositionsandtoothmorphology. Inaddition,fossilrecordsclearlyshowthat2makos However,inspiteofthesesimilarities,Compagno aresistertaxa(12). defendedLamniformesasmonophyletic.Inaddition,in BasedonCompagno’sconclusionofthese2 1988,12ordersofrecentelasmobranchs,whichwere hypotheses,CarcharodonandIsurushavebeenidentified consideredmonophyletic,weredividedinto2major assistertaxa,while,asalternativelysuggested,thefact monophyleticgroupsbyCompagno;theGaleomorphii thatCarcharodonandLamnahavebeenidentifiedas andSqualea.Onceagain,Lamniformeswereplacedin sistertaxacannotbeignored.Onepossiblereasoncould Galeomorphii.Whenheexplainedthelamnoid bethatinthedistantpastall3generaseparatedfrom assemblage,Compagnoproposed5families eachotherwithinashortperiodtime.Thispossibilityis (Mitsukurinidae,Odontospididae,Pseudocarcharinidae, supportedbytheestimationsofsequencedivergence, Megachasmidae,andAlopidae)and3subfamilies whichareverysimilartoeachother(Isurus-Carcharodon (Alopiinae,Cetorhininae,andLamninae,whichincludes =7.1%,Isurus-Lamna =8.4%,andCarcharodon-Lamna Carcharodon,Isurus,andLamna)insidethisorder.Some =6.2%)(9). researcherssupportedthis;othersdidnot(6).Several Inaddition,Martintriedtoelucidatetherelationship similarstudieshavebeenperformedonthissubject,and withinthefamilyLamnidaebyparsimonyphylogenetic thisrecentelasmobranchclassificationhasbeenwidely analysisofthemitochondrialcytochromebgene.The accepted,withthedifferencesofLamninaebeinga resultsstronglysuggested(100%)thatthefamily subfamilyinsteadoffamilyinthecurrentclassification. Lamnidaeismonophyletic.Themonophylyofthe2 Thefirstappearanceofeachlineagecanbefoundin speciesofIsurus,andthemonophylyofIsurusand theknownfossilrecords.Onegroupofsharksinthe Carcharodonweresupportedwithreasonablystrong orderLamniformesareverywellpreservedinthefossil values(85%-97%and78%-88%,respectively)in records.Fromtheserecords,whichprovideinformation additiontothefindingthatasasistertaxaLamnawasthe aboutratesandpatternsofmolecularevolution, mostancestralextantgenusofthisfamily(corroborated independentphylogenetichypothesescanbemade. byCompagno(7))(9).Thesefindings,indicatingthatthe Moleculardata(DNAoraminoacidsequences)also familyLamnidaeisamonophyleticgroup,weresupported provideextensiveinformationabouttherelationships. usingrecombinantactivationgene(Rag-1)phylogenetic Agreementontheoriginationandthetimeofdivergence analysisbyMartin(13)andwiththemitochondrialNADH betweenthemoleculardataandfossilrecordcanbeused 2andcytochromebgenesbyNayloretal.(2). inthepropositionofthebesthypothesis. Inanotherstudy,byMartinetal.(14),theSSRlocus Therearestilluncertaintiesabouttherelationship (Loc6)wasamplifiedusingprimersLoc6F5´-ATTGTT withinthefamilyLamnidaeandalternativehypotheses TCGTGGCCTAGGTG-3´andLoc6R5´-AGCCACATC havebeensuggested.Forexample,onehypothesis GATAATCCCAG-3´fromLamniformsharks,andseveral proposedbyCompagnoindicatesthatIsurus(mako differentlengthdeletionswereobtainedintheregion sharks)andCarcharodonaresistertaxa,andLamna flankingtherepeatmotif,ofwhichonewaspresentinall (porbeagleandsalmonsharks)isthemostancestral speciesoftheLamnidae. genusofthefamily,basedonasurveyofmorphological TheorderLamniformesiscommonlyconsideredthe characteristics(7). sistergroupofCarcharhiniformes,butrecentstudies 110 M.DOSAYAKBULUT basedonmoleculardatahaveledtotheproposalofan PhylogeneticAnalysis alternativehypothesisinwhichLamniformesand Anapproximately1100-bpmitochondrialcytochrome Orectolobiformes(carpetsharks)areassignedasthe bgenenucleotidesequencewasobtainedfromGenBank sistergroupsofCarcharhiniformes(15).Similarly, andaligned.Thebestpossiblealignmentwasusedina Winchelletal.proposedacloserelationshipamong treeconstruction.Thesequencewasloadedintothe lamniforms,carcharhiniforms,andorectolobiformsbased Eyeballsequenceeditor(20).Thesequencealignments on12Sand16SrRNA,tRNAvaline,andmitochondrial wereformedusingtheMEGALIGNprogramwithinthe cytochromebgenemolecularanalysis(16). DNASTARpackageandadjustmentsweremadevisually. Amolecularphylogeneticstudyofthemitochondrial GenBankaccessionnumberswereasfollows: Alopias 12S-16SlocusandtRNAvalinebyDouadyetal.also vulpinus cytochromebresult:U91442;Isurusoxyrinchus supportedtheLamniform-Carcharhiniformassociation cytochromebresult:L08036; Isuruspaucus cytochrome (17). bresult:L08037; Carcharodoncarcharias cytochromeb result:L08031; Lamnanasus cytochromebresult: Phylogeneticdistributionofdifferentmodesof L08038;Odontaspisferox cytochromebresult:U91445; reproductionalsoputthelamniforms,carcharhiniforms, Lamnaditropis cytochromebresult:U91438(2). andorectolobiformssharkorderstogether(18). Thedatawereanalyzedusingmaximumparsimony Thesepreviousstudiesreportdiverseresultsabout (MP)methodswithinthePHYLIPv.3.5cprogram(21). therelationshipamongthefamilyLamnidae.Thereseems Theanalysesreliabilitywaslatertestedbybootstrapping tobeuncertaintyaboutwhichspeciesisthesistertaxon (22)with1000replicationsofthedata.Similarly, totheIsurus(makos).Inthisstudy,tofindanaccurate transversionparsimony(TP)wasappliedtodatathat answertothefamilylamnidaeinterrelationshipthe includedonlytransversionsignalsbymanuallyconverting mitochondrialcytochromebgeneof2makos( Isurus itintopurinesandpyrimidinesusingMPmethodswithin paucus and Isurusoxyrinchus ),theporbeagle( Lamna thePHYLIPv.3.5cprogram(21).Thereliabilitywas nasus),salmonshark( Lamnaditropis),andwhiteshark testedbybootstrapping(22)with1000replicationsof (Carcharodoncarcharias),inadditionto2outgroups,the
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