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Systematics of the Anopheles Barbirostris Species Complex (Diptera: Culicidae: Anophelinae) in Thailand

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Systematics of the Anopheles Barbirostris Species Complex (Diptera: Culicidae: Anophelinae) in Thailand bs_bs_banner Zoological Journal of the Linnean Society, 2015, 174, 244–264. With 6 figures Systematics of the Anopheles barbirostris species complex (Diptera: Culicidae: Anophelinae) in Thailand KRITSANA TAAI1 and RALPH E. HARBACH2* 1Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 2Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Received 31 July 2014; revised 4 December 2014; accepted for publication 16 December 2014 This study deals with five species of the Barbirostris Complex of Anopheles subgenus Anopheles that are known to occur in Thailand. Three new species of the complex, Anopheles dissidens sp. nov., Anopheles saeungae sp. nov., and Anopheles wejchoochotei sp. nov., are characterized and compared with Anopheles barbirostris van der Wulp and Anopheles campestris Reid based on specimens of molecularly identified progeny broods. For practical purposes, the five species are essentially isomorphic and can only be unequivocally identified from di- agnostic mitochondrial and ribosomal DNA sequences. Based on overall morphological similarity, An. campestris is considered to be a member of the Barbirostris Complex rather than a separate member of the Barbirostris Sub- group. The molecular data, mitotic karyotypes, bionomics, and distributions of the species are reviewed and dis- cussed. It is concluded that integrated molecular epidemiological studies of the complex throughout the Oriental Region are needed to unambiguously elucidate the individual species and their relation to disease. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 244–264. doi: 10.1111/zoj.12236 ADDITIONAL KEYWORDS: Bayesian analysis – cryptic species – molecular systematics – morphological comparison – morphology – mosquitoes – mtDNA – new species – rRNA. INTRODUCTION Three of these species are characterized, formally named, and contrasted with An. barbirostris in this paper. Based Anopheles (Anopheles) barbirostris van der Wulp is the on overall morphological similarity, we also include and nominotypical member of a medically important group recognize An. campestris as a member of the Barbirostris of 14 formally named species (Barbirostris Group) in Complex. the Oriental Region (Harbach, 2013). Twelve of these species are classified into subgroups, the Barbirostris and Vanus Subgroups. The Barbirostris Subgroup in- MATERIAL AND METHODS cludes five species described by Reid (1962), includ- ing Anopheles campestris Reid and two nominal species SPECIMENS AND MORPHOLOGY of the Barbirostris Complex, Anopheles barbirostris and Specimens of the new species described below were Anopheles vanderwulpi Townson & Harbach. Based on reared from progeny broods obtained from wild- the results of cross-mating studies and analyses of caught blood-fed females collected in various loca- mitochondrial and ribosomal DNA sequences (Saeung tions in Thailand and Indonesia. The progeny broods et al., 2007, 2008; Paredes-Esquivel et al., 2009; were identified to species based on sequences for the Suwannamit et al., 2009; Thongsahuan et al., 2009; cytochrome c oxidase subunit I (COI) of mitochondrial Townson et al., 2013), the Barbirostris Complex is cur- DNA (mtDNA) and the internal transcribed spacer 2 rently known to include at least four additional species. (ITS2) of ribosomal DNA (rDNA) obtained using the procedures of Saeung et al. (2008), Paredes-Esquivel et al. (2009), and Suwannamit et al. (2009). Larvae were *Corresponding author. E-mail: [email protected] individually reared to provide adults with associated 244 © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 244–264 THE ANOPHELES BARBIROSTRIS COMPLEX 245 larval and pupal exuviae. These specimens, individ- Tissue Kit (QIAGEN). The ribosomal ITS2 region and ually reared specimens that comprise the type series the mitochondrial COI gene were amplified using the of An. campestris, and specimens unequivocally iden- primers and thermal profiles described in Saeung et al. tified from their COI sequence as An. barbirostris in (2007) and Suwannamit et al. (2009). the study of Townson et al. (2013), were used for the comparative anatomical study. Adults were studied using SEQUENCE ALIGNMENT AND PHYLOGENETIC ANALYSES stereomicroscopy and simulated natural light. Larval and pupal chaetotaxy and dissected male genitalia were The DNA sequences were aligned using CLUSTAL W studied using bright-field microscopy. The morphologi- (Thompson, Higgins & Gibson, 1994) in BioEdit v. 7.0.5.3 cal terminology used herein is defined in the Anatomi- (Hall, 1999). Gap sites were excluded from the follow- cal Glossary of the Mosquito Taxonomic Inventory (http:// ing analysis. The Kimura two-parameter (K2P) model mosquito-taxonomic-inventory.info/). The symbols Ǩ, ǩ, was employed to calculate genetic distances (Kimura, E, Le, Pe, P, and L used in the synonymies/literature 1980), implemented in Molecular Evolutionary Genet- summaries, Material examined, and Type series rep- ics Analysis (MEGA) v. 6.0 (Tamura et al., 2013). Bayes- resent female(s), male(s), egg(s), larval exuviae, pupal ian analysis was conducted with MrBayes 3.2 (Ronquist exuviae, pupae, and fourth-instar larvae, respective- et al., 2012) by using two replicates of 1 000 000 gen- ly. An asterisk (*) following these symbols indicates erations with the nucleotide evolutionary model. The that at least part of the life stage is illustrated in the best-fit model was chosen for each gene separately using corresponding publication. the Akaike information criterion (AIC) in MrModeltest Measurements (e.g. wing length) in millimeters (mm) v. 2.3 (Nylander, 2004). The general time-reversible (GTR) and counts (e.g. number of setal branches) are given with gamma distribution shape parameter (G) was the as a range followed by the mean or mode, respective- best-fit model for the ITS2 and COI sequences. Bayes- ly, in parentheses. Variation observed in anatomical ian posterior probabilities were calculated from the con- features of adult females and male genitalia was ana- sensus tree after excluding the first 25% of trees as lysed by one-way analysis of variance (ANOVA). Dif- burn-in. Specimens used in the phylogenetic analyses, ferences among the five species treated herein were along with GenBank accession numbers for their ITS2 compared using Scheffé’s method. Data for thoracic setal and COI sequences, are listed in Table S1. Anopheles groups were compared using the Kruskal−Wallis test. (Cellia) dirus Peyton & Harrison was used as outgroup All data were analysed using SPSS v. 16.0 for Windows in the analyses of both ITS2 and COI. (Chicago, SPSS Inc.). Statistical significance was set < at P 0.05. SYSTEMATICS ANOPHELES (ANOPHELES) BARBIROSTRIS CYTOTAXONOMY VAN DER WULP The cytotaxonomy of members of the Barbirostris Group Anopheles barbirostris van der Wulp, 1884 (Ǩ). Holotype is based on mitotic chromosomes found in the neural Ǩ: Mount Ardjoeno, Java, Indonesia (Nationaal ganglia of fourth-instar larvae derived from isoline colo- Natuurhistorisch Museum, Leiden, Netherlands). nies. Metaphase karyotypes observed in the brain cells Anopheles martini Laveran, 1902 (Ǩ). Type local- are characterized by the size and shape of the X and ity: near Pursat, Cambodia (Institut Pasteur, Y chromosomes. The karyotypic forms listed for the Paris). It is not possible to know for certain whether species described herein consist of combinations for the or not this nominal species is conspecific with following chromosomal designations: X1 (small An. barbirostris or another member of the Barbirostris metacentric chromosome), X2 (medium submetacentric Complex. chromosome), X3 (large submetacentric chromosome, Anopheles barbirostris innominata Stoker & Waktoedi same as X2 but slightly longer), Y1 (subtelocentric Koesoemawinangoen, 1949 (Ǩǩ). Type locality: [acrocentric] chromosome), Y2 (large submetacentric Sulawesi, Indonesia (type non-extent). This nominal chromosome),Y3 (large submetacentric or metacentric form may be a distinct member of the Barbirostris chromosome with large block of heterochromatin at the Complex. distal end of the long arm), Y4 (medium metacentric Anopheles (Anopheles) barbirostris in part of chromosome), Y5 (small metacentric chromosome), and Bonne-Wepster & Swellengrebel, 1953 (Indonesia, Ǩ* Y6 (large subtelocentric chromosome). ǩ* L*); Reid, 1962 (Indonesia, Malaysia, Thailand, Ǩ* ǩ E* L P*, taxonomy); Reid, 1968 (Malaysia, Borneo, Ǩ* ǩ* E L* P*, taxonomy, biology); Harrison & Scanlon, DNA EXTRACTION AND AMPLIFICATION 1975 (Thailand, Ǩ* ǩ* L* P*, taxonomy); Reid, DNA was extracted from individual adult female mos- Harrison & Atmosoedjono, 1979 (Indonesia, Malay- quitoes of progeny broods using a DNeasy Blood and sia, Thailand, Ǩ* L P* morphology, taxonomy). © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 244–264 246 K. TAAI AND R. E. HARBACH Anopheles barbirostris in part (?) of Harrison, ments and statistical analysis of selected anatomical Rattanarithikul & Mongkolpanya, 1988 (Thailand, A features compared with other species of the complex L P morphology); Ndoen et al., 2010, 2011 (West Timor, in Tables 1 and S2, respectively. Java, ecology, bionomics). Anopheles barbirostris form A in part of Baimai, Head: Vertex dark-scaled with patch of pale scales before Rattanarithikul & Kijchalao, 1995 (Thailand, meta- interocular space; interocular space with mostly dark phase karyotype). setae
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