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Higher-Level Phylogeny of Mosquitoes (Diptera: Culicidae): Mtdna Data Support a Derived Placement for Toxorhynchites

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Higher-Level Phylogeny of Mosquitoes (Diptera: Culicidae): Mtdna Data Support a Derived Placement for Toxorhynchites Higher-level phylogeny of mosquitoes (Diptera: Culicidae): mtDNA data support a derived placement for Toxorhynchites ANDREW MITCHELL, FELIX A. H. SPERLING and DONAL A. HICKEY Insect Syst Evol Mitchell, A., Sperling, F. A. H. & Hickey, D. A.: Higher-level phylogeny of mosquitoes · · (Diptera: Culicidae): mtDNA data support a derived placement for Toxorhynchites. Insect Syst. Evol. 33: 163-174. Copenhagen, July 2002. ISSN 1399-560X. We assess the potential of complete coding sequences of the mitochondrial cytochrome oxi­ dase genes (COl and COil) and the intervening tRNA-Leucine gene for use in mosquito high­ er-level systematics, and apply this data to an outstanding question: the phylogenetic affinities of Toxorhynchites. Traditionally placed in its own subfamily and regarded as sister group to Culicinae, recent morphological data instead have suggested that this distinctive genus belongs well within the Culicinae. Published molecular systematic studies seemingly conflict with this new morphological data or are ambiguous. The mitochondrial gene data that we pres­ ent show good potential for elucidating suprageneric relationships in Culicidae, and strongly support the placement of Toxorhynchites well within the Cnlicinae. Reexamination of pub­ lished data sets suggests that there is no substantive conflict among data sets on this issue. Andrew Mitchell, School of Molecular and Cellular Biosciences, University of Natal, Private Bag XOl, Scottsville, 3209, South Africa ([email protected]). Felix A. H. Sperling, Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada ([email protected]). Donal A. Hickey, Department of Biology, University .of Ottawa, Ottawa, Ontario, KlN 6N5, Canada ([email protected]). Introduction tionships among subfamilies by Harbach & Mosquito taxonomy has received intense attention Kitching ( 1998). However, their novel results have as a direct result of the immense medical impor­ yet to gain wide acceptance. This is largely be­ tance of many mosquitoes as vectors of disease­ cause of apparent conflict between their data and causing organisms. The realisation that accurate published data sets, both morphological and delimitation of species boundaries and an in-depth molecular. In this study we assess the potential of knowledge of geographic variation are essential . mitochondrial DNA sequence data for resolving for vector control has resulted in a focus on spe­ contentious issues in mosquito higher-level sys­ cies-level taxonomy in Culicidae. The higher-level tematics by examining the phylogenetic placement phylogeny of Culicidae is much more poorly of Toxorhynchites. understood. Among the reasons for this is the im­ Recent classifications of Culicidae recognize portance of nomenclatural stability in this impor­ three subfamilies: Anophelinae, with 3 genera, tant group, which understandably has led to con­ Culicinae, with 34 genera arranged in 10 tribes, -servative nomenclature. One could also argue, and Toxorhynchitinae, with a single genus, Toxo­ however, that the widespread importance of mos­ rhynchites. The distinctiveness of Toxorhynchites quitoes is in itself a strong motivation for provid­ was recognized early on, because the species are ing an up-to-date classification that more closely among the largest and most spectacular of all mos­ reflects phylogeny. Nevertheless, the earlier phe­ quitoes. Toxorhynchites females do not take blood netic work has largely pre-empted later cladistic meals, and oviposit in small, natural plant contain­ studies, and most systematists have followed the ers where the larvae are predatory (Steffan & classification of Edwards (1932) with little modi­ Evenhuis 1985). Toxorhynchites species have even fication. Rigorous phylogenetic methodology has been used as biological control agents of other only recently been applied to the problem of rela- mosquitoes, though with limited success (Steffan © Insect Systematics & Evolution (Groups 6 & 7) 164 Mitchell, A. et al. INSECT SYST. EVOL. 33:2 (2002) & Evenhuis 1981). Despite these differences, a material are listed in Tab. 1. Specimens were col­ few authors considered the apparent peculiarity of lected in the wild or taken from laboratory the Toxorhynchitinae to have been overempha­ colonies and then either frozen live at -70°C or sized. Belkin (1962), for example, treated the preserved a few days in 95% ethanol before being group as a tribe of equal rank to the ten tribes of frozen at -70°C. Identifications of wild-collected Culicinae, and considered them closely related to material were provided by D. M. Wood {Agri­ the Sabethini. This hypothesis was supported by culture and Agri-Food Canada, Ottawa, Canada). Harbach & Kitching's (1998) morphology-based Our taxon sample included eleven mosquito cladistic analysis of all mosquito genera. species, including four anophelines, five culicines Molecular data, in contrast, have seemingly sup­ (from four tribes), and two toxorhynchitines. The ported the traditional placement of Toxorhynchites outgroup comprised two species, including a rep­ (Besansky & Fahey 1997) or have been equivocal resentative of Chaoboridae, most likely the sister (Miller et al. 1997).~ group of Culicidae (Oosterbroek & Courtney Which of these alternative placements for 1995) or at least very closely related (Pawlowski Toxorhynchites is better supported? We present et al. 1996), and a more distantly related culico­ sequence data .of the complete mitochondrial morph (a blackfly, Simuliidae). Published se­ cytochrome oxidase genes, COI and COil, and the quences .were obtained from GenBank for Ano­ intervening tRNA-Leucine gene (a total of 2.3kb ), pheles quadrimaculatus (Mitchell et al. 1993) and in order to assess the utility of these genes for A. gambiae (Beard et al. 1993). All other se­ mosquito higher-level phylogenetics, and to pro­ quences are new data. vide additional data bearing on this problem. Laboratory protocols. - For most specimens, DNA was extracted from individual specimens Materials and methods using a phenol!chloroform procedure as described by Sperling et al. (1994). For two specimens (Sa­ Abbreviations. - CO, cytochrome oxidase; GTR, bethes L-yaneus and Toxorhynchites sp.) DNA was general time reversible; ML, maximum likelihood; extracted using the Qiagen DNeasy Tissue Kit MP, maximum parsimony; mp, most parsimonious. (Qiagen Inc., Valencia, California). PCR was Taxon sampling. - Taxa sampled and sources of accomplished using the protocol of Sperling et al. Table 1. Taxon sampling. Taxon Source• Culicidae Anophelinae Anopheles (Anopheles) earlei Ottawa, Canada; D. M. Wood AF425843 Anopheles (Anopheles) quadrimaculatus Mitchell et al. (1993) NC000875 Anopheles (Cellia) gambiae Beard et al. ( 1993) NC002084 Anopheles (Cellia) stephensi LC, University of Maryland; V. Kulasekara AF425844 Culicinae Aedes atropalpus LC, University of Ottawa; T. Amason AF425845 Aedes aegypti LC, University of Ottawa; D. Hickey AF425846 Culex tarsalis LC, Queens University; V. Walker AF425847 Culiseta impatiens Ottawa, Canada; D. M. Wood AF425848 Sabethes cyaneus LC, University of Notre Dame; N. Besansky AF425840 Toxorhychitinae Toxorhynchites rutilus York Co., Pennsylvania; D. M. Wood AF425849 Toxorhynchites sp. Vietnam; D.C. Currie AF425850 Chaoboridae Chaoborus sp. Ottawa, Canad~; D. M. Wood AF425842 Simuliidae Cnephia dakotensis Ottawa, Canada; D. M. Wood AF425841 •LC =Laboratory colony bThe complete alignment is also available from TreeBase (http://www.herbaria.harvard.edultreebase/). INSECT SYST. EVOL. 33:2 (2002) (1994). the end primers TY-J-1460 (=K698: pe1formed using identical protocols. All phyloge­ 5' -TAC AAT ITA TCG CCT AAA CIT CAG CC netic analyses were performed PAUP* ver­ and TK-N-3782 5'- GAG ACC AIT sions 4.0b4a and 4.0b8 Altivec (Swofford 1999). ACT TGC ITT CAG TCA TCT -3') and a variety lnc:on:gruem:e length difference (ILD) tests of primers developed by us consisted of 1000 heuristic from a comparison of GenBank sequences of etitions, each with 10 random addition sequelltces Vrt?sn.vmta yakuba, gambiae, and A. of taxa. A branch-and-bound maximum parsimony quadrimaculatus. For Cnephia. da- (MP) search was performed on our rntDNA data kotensis, Chaoborus sp., and Sabethes cyaneus, set. Further MP on our and all other the above end primers did not amplification MP analyses, of 1000 random addition products. For these taxa we developed far- sequences of ther out from the COIICOIT region. upstream sequences and, in primer used for Cnephia and Sabetl}.es was TW-J- genes, also on the inferred amino acid seaner1ces 1305 5'- GIT AAA TAAA'CT AAT AGC (740 characters). analyses CIT CAA AGC TG -3') and for Chaoborus was 1000 repetitions, each with 10 random addition TY-J-14601 5'-ITACAATTTCTTACT sequences of taxa. Constraint searches were car­ TAA GTT CAG CC -3'). The downstream ried out for each data set to determine the number used for both and Chaoborus was of additional steps needed to accommodate alter­ 3862 (5'- GGC CGT CTG ACA AAC TAA TGT native phylogenetic hypotheses. Bremer support TAT -3') from Simonet al. (1994). For most spec­ (or 'decay') indices (Bremer 1988) were calculat­ imens PCR · were sequenced directly ed for the morphological data set & Kit- using the Taq DyeDeoxyT111 Terminator Cycle 1998). Se(tUeJ:tciilg System (Applied Biosystems, Inc.) To assess the effects of biased base composition and fractionated on an ABI 373 automated DNA oh1vlo:£!:el1tV reconstruction we dis- sequencer. For two specimens ana!vs<~s based on the LogDet et
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