Combined Molecular Phylogenetic Analysis of the Orthoptera
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Syst. Biol. 48(2):233–253, 1999 CombinedMolecular Phylogeneti cAnalysisof theOrthoptera (Arthropoda,Insecta) and Implications for Their Higher Systematics P. K. FLOOK,1 S. KLEE, AND C. H. F. ROWELL ZoologyInstitute, University of Basel, 4051-Basel,Switzerland Abstract.—Aphylogenetic analysisof mitochondrial andnuclear rDNA sequences fromspecies of all the superfamilies of the insect orderOrthoptera (grasshoppers,crickets, andrelatives) conrmed thatalthough mitochondrial sequences provided goodresolution of the youngestsuperfamilies, nuclear rDNA sequences were necessaryto separatethe basalgroups. To try to reconcile these datasets into asingle, fully resolved orthopteranphylogeny ,we adoptedconsensus andcombined datastrategies. Theconsensus analysisproduced apartially resolved tree thatlacked several well- supported features of the individual analyses.However, this lackof resolution was explained by anexamination of resampled datasets, which identied the likely source of error asthe relatively short length of the individual mitochondrial datapartitions. Inasubsequentcomparison in which the mitochondrial sequences were initially combined,we observed less conict. Wethen used two approachesto examinethe validity of combiningall of the datain asingle analysis:comparative analysisof trees recovered fromresampled datasets, andthe application of arandomizationtest. Be- cause the results did not point to signicant levels of heterogeneity in phylogenetic signalbetween the mitochondrial andnuclear datasets, we therefore proceeded with acombined analysis.Recon- structing phylogenies underthe minimum evolution andmaximum likelihood optimality criteria, we examinedmonophyly of the majororthopteran groups, using nonparametric and parametric bootstrapanalysis and Kishino– Hasegawa tests. Our analysissuggests that phylogeny reconstruc- tion underthe maximumlikelihood criteria is the most discriminating approachfor the combined sequences. Theresults indicate, moreover, thatthe caeliferan Pneumoroideaand Pamphagoidea, aspreviously suggested,are polyphyletic. TheAcridoidea is redened to include all pamphagoid families other thanthe Pyrgomorphidae,which we propose should beaccorded superfamily status. [Combinedanalysis; insect phylogeny;molecular evolution; Orthoptera;ribosomal DNA.] Wehaveused phylogenies reconstructed The failure of these analysesto generate fromnucleotide sequences toexamine the fully resolvedphylogenies maystem from evolutionaryhistory of the insectorder Or- the antiquityof the Orthoptera.Divergence thoptera(grasshoppers, crickets, and rel- datesof the majorgroups are estimated to atives)(Flook andRowell, 1997a, 1997b, range overa period of ~200million years, 1998).Of particularinterest are relationships withfossils of the oldestgroups appearing of severalof the higher taxa,and we have in the Permian(Carpenter andBurnham, attemptedto relate our results to existing 1985).Consequently ,althoughthe relatively systematicdisputes. The molecularphylo- rapidly-evolving mitochondrialsequences genies arewell suitedto this task and have haveproven valuablefor examining com- the potentialto resolve several outstanding parativelyrecent events(Flook andRow- problemsconcerning the ecology,character ell, 1997b),the basalbranching patternsof evolution,and biogeographic distributionof the Orthopteraare resolved only by the member taxa.However, the successof these moreslowly evolving nuclearribosomal analyseshas been limitedsince, on their RNAgene sequences (Flook andRowell, own,the different sequences haveproven in- 1998).In contrast,these nuclearsequences adequatefor reconstructing phylogeny over arealmost invariant in the morerecently the whole range oforthopteran evolution. evolved groups,and wewere previously un- Becauseof this, we haveso farbeen unable able todetect signi cant phylogenetic signal toreduce the ndings ofour work to a single amongthe four youngest caeliferan super- schema. families.On the basisof these results,we ex- pect thatthe datasets contain enough phy- logenetic signalbetween themto determine 1 Address correspondence to Dr. P.K.Flook,Zool- ogisches Institut, Rheinsprung9, 4051-Basel, Switzer- mostof the majorfeatures of orthopteran land.E-mail: [email protected]. phylogeny in asingle analysis.The purpose 233 234 SYSTEMATICBIOLOGY VOL. 48 of the workreported here wasto identify hood(ML) optimality,weobtaina phyloge- aneffective strategyfor resolving the or- netic scheme in which the majorityof nodes thopteranphylogeny fromthe three data areresolved. sets. Twofundamentally different approaches fortreating multiple phylogenetic datasets arecommonly applied: consensus,and com- MATERIALS AND METHODS bined analyses.Both of these strategieshave been criticized(Bull et al.,1993; de Queiroz, Samples 1993),and selection of one overthe otheris Samples fromall the orthopteransuper- complicated.An argumentin favorof com- familieswere included in thisstudy .In the bining datais that, because mostreconstruc- suborderCaelifera (shorthorned grasshop- tionmethods are consistent (for mostun- pers) seven superfamilies arecommonly derlying tree shapes),an analysis is more recognized(see Dirsh,1975; Rentz, 1991): likely torecover the correctphylogeny as Tridactyloidea(false molecrickets, sand dataare added. On the otherhand, phylo- gropers);T etrigoidea(pygmy grasshoppers, genetic reconstructioncan become compli- grouselocusts); Eumastacoidea (monkey catedwhen datathat evolve atvery differ- grasshoppers,false stick insects); Pneu- ent rates(e.g., mitochondrialand nuclear moroidea( ying gooseberries,desert long- DNA) arecombined in asingle analysis.As horned grasshoppers,razor-back bush- hasbeen demonstrated,when heterogene- hoppers); Pamphagoidea(rugged earth ityexists in phylogenetic signalfrom dif- hoppers, true bush-hoppers); Acridoidea ferent datapartitions, the overallsignal is (grasshoppers,locusts); and T rigonoptery- sometimesdiminished afterpooling ofdata; goidea.In the otherorthopteran suborder , in suchcases, data combination should be Ensifera(long-horned grasshoppers,katy- avoided(Bull et al.,1993; de Queiroz,1993). dids,crickets), we sampledall four super- Bull et al.(1993), discussing the alternatives families(following the higher classication foranalyzing multiple datasets, maintain ofGorochov ,1995b):Tettigonioidea (bush- thata combining ofdata should be preceded crickets,katydids); Hagloidea (hump- byasearchfor any con ict between the in- winged crickets);Stenopelmatoidea (cave dividualdata sets. crickets,Jerusalem crickets,wetas); and Here we estimaterelationships among Grylloidea(true crickets,mole crickets). In orthopteransfrom new andpreviously pub- additionwe used outgrouptaxa from three lished moleculardata and, in doing so, relatedorders: Phasmida (walking sticks); examine severalimportant aspects of phy- Blattodea(cockroaches); and Grylloblat- logeny reconstruction.First, we considerthe todea(ice-crawlers). A full listof the mate- choiceof reconstruction method in situa- rialused in thisstudy is given in Table 1.The tionswhere contrastingphylogenetic lev- seven taxain which sequences were deter- els areexamined simultaneously.Second, mined forthe rsttime were Rhainopomma wecomparethe use ofboth consensus and montanum (Caelifera, Acridoidea,Lentu- datacombination approaches for analyz- lidae), anunidenti ed species of Systella ing the mitochondrialand nuclear riboso- fromBorneo (Caelifera, Trigonopterygoid- malDNA (rDNA) sequences. Wesuggest ea,T rigonopterygidae), Tanaocerus koebeli thatconsensus methods are too conservative (Caelifera, Pneumoroidea,T anaoceridae), forthe treatmentof the orthopterandata. Xyronotus aztecus (Caelifera, Pneumoroidea, Wedemonstratethat combining nuclearand Xyrolnotidae), Physemacrisvariolosa (Caeli- mitochondrialDNA (mtDNA) sequences in fera,Pneumoroidea, Pneumoridae), Comi- asingle analysisis legitimate, in spite of the cus campestris (Ensifera,Stenopelmatoidea, factthat the sequences areevolving atdif- Stenopelmatidae),and Ceuthophiluscarlsbad- ferent rates.Reconstructing trees from the ensis (Ensifera,Stenopelmatoidea, Rhaphid- combined dataset under the criteriaof min- ophoridae).Procedures for collection and imumevolution (ME) andmaximum likeli- storageof materialand for DNA isolation 1999 TABLE 1. Taxonomic sample examined in this study. The higher taxonomic groups of the Caelifera and Ensifera identied here correspond to those listed by Dirsh (1975) and Gorochov (1995b), respectively. The Acridomorphoidea sensu Dirsh (1975) corresponds to the superfamilies Acridoidea, Pamphagoidea, Pneumoroidea, and Trigonopterygoidea. EMBL accession nos. Order Suborder Superfamily Family Genus Species 12S 16S 18S Orthoptera Caelifera Acridoidea Acrididae Gomphocerippus rufus Z93247 Z93285 Z97591 FLOOK Acrida turrita Z97596a Z97612a Z97560 Oedipoda coerulescens Z93255 Z93293 Z97573 a a a Lentulidae Rhainopomma montanum Z97601 Z97618 Z97581 ET Pamphagoidea Pamphagidae Glauia terrea Z93258 Z93296 Z97568 Batrachotetrix sp. Z93259 Z93297 Z97590 AL.— Pyrgomorphidae Prosphena scudderi Z93261 Z93299 Z97579 a a Pyrgomorpha conica Z97600 Z97616 Z97580 PHYLOGENETIC Pneumoroidea Pneumoridae Bullacris membracioides Z93264 Z93302 Z97562 Pneumora inanis Z93265 Z93303 Z97577 Physemacris variolosa Z97599a Z97615a Z97576a Tanaoceridae Tanaocerus koebeli Z97605a Z97621a Z97586a Xyronotidae Xyronotus aztecus Z97607a Z97623a Z97588a Trigonopterygoidea Trigonopterygidae Systella rafesi Z97604a Z97620a Z97585 Systella sp. Z97603a Z97619a Z97584a Eumastacoidea Proscopiidae Prosarthria teretrirostris Z93266