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Advance Publication by J-STAGE Advance Publication by J-STAGE Japanese Journal of Infectious Diseases Molecular characterization of mosquitoes (Diptera: Culicidae) of Northwestern Iran using rDNA-ITS2 Farahnaz Khoshdel-Nezamiha, Hassan Vatandoost, Mohammad Ali Oshaghi, Shahyad Azari-Hamidian, Reza Arabi Mianroodi, Farrokh Dabiri, Masoomeh Bagheri, Olle Terenius, and Ali Reza Chavshin Received: June 8, 2015. Accepted: November 10, 2015 Published online: January 8, 2016 DOI: 10.7883/yoken.JJID.2015.269 Advance Publication articles have been accepted by JJID but have not been copyedited or formatted for publication. Title: Molecular characterization of mosquitoes (Diptera: Culicidae) of Northwestern Iran using rDNA-ITS2 Short Title: ITS2 of mosquitoes of Northwestern Iran Authors: Farahnaz Khoshdel-Nezamiha1,2, Hassan Vatandoost3, Mohammad Ali Oshaghi3, Shahyad Azari-Hamidian4, Reza Arabi Mianroodi5, Farrokh Dabiri2 , Masoomeh Bagheri6, Olle Terenius7, Ali Reza Chavshin1,2* Addresses plus emails: 1Research Center of Social Determinants of Health, Urmia University of Medical Sciences, Urmia, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran 3Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 4School of Health, Guilan University of Medical Sciences, Rasht, Iran 5 The production and research complex, Pasteur Institute of Iran, Tehran, Iran 6 Student Research Committee, Urmia University of Medical Sciences, Urmia, Iran 7 Department of Ecology, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden Corresponding author: Dr. Ali Reza Chavshin , Urmia University of Medical Sciences, Urmia, Iran Email: [email protected],Accepted [email protected] Manuscript Tel/Fax: +98 443 2770047 Mob: +989125010147 Keywords: Culiseta longiareolata, Culex hortensis, molecular phylogeny, ITS2, Iran 1 Abstract Several mosquito species are vectors of disease; however, to understand their role in disease transmission, accurate species identification is of particular importance. Morphological-based identification remains the main method, but molecular techniques have emerged as a tool for identification of closely related species. In this study, mosquitoes of the West Azerbaijan Province in Northwestern Iran were characterized based on their rDNA-ITS2 sequences. Nine populations of Six species of mosquitoes belonging to Anopheles, Culex, Culiseta and Ochlerotatus genera were studied. For the first time, the ITS2 sequences of Culiseta longiareolata and Culex hortensis are reported. In addition, ITS2 of Culex theileri and Ochlerotatus caspius are for the first time reported from Iran. phylogenetic analysis based on ITS2 fragment showed that both Subfamilies (Anophelinae and Culicinae) of this family (Culicidae) could be differentiated successfully, and also in Genus Anopheles, both the studied Subgenera (Anopheles and Cellia) were separated. About the divergence of differently studied Genera (Culex., Culiseta and Ochlerotatus), the analysis showed that Genera Culiseta, Ochlerotatus and Culex. have been diverged separately. Accepted Manuscript 2 Introduction Mosquitoes transmit several important diseases and can be considered as the most important insect vectors. An accurate identification of the mosquito species will lead towards understanding the role of each species in the disease transmission cycle. In turn, this leads to effective control programs designed according to the bio-ecology of each species (1). Morphological-based identification remains the main method, but molecular techniques have emerged as a tool for identification of closely related species. The molecular marker rDNA- ITS2 is used in molecular taxonomy for separating sibling species (2), in phylogeny for establishing evolutionary relationships among mosquito species (3), and in phylogeography and population genetics which aims at assessing mosquito geographic distribution (4). Molecular studies have been carried out in order to characterize the Culicidae species of Iran and taxonomic clarification in some problematic situations, e.g. different species of Iranian Oriental-Palearctic-Afrotropical Members of Genus Anopheles (5), Anopheles stephensi (6), An. Hyrcanus (7), An. fluviatilis (8), An. superpictus (9), An. maculipennis (10). According to the mentioned studies, carrying out a study considering species from different taxa of Culicidae family, seems to be neccesary. The West Azerbaijan Province in northwestern Iran is an important biogeographic region being the corridor between Europe, Africa and Asia. This province has common border line with four foreign countries: Armenia, Azerbaijan, Iraq and Turkey. In this study, we characterized mosquitoes collected from different locations of the West AzerbaijanAccepted Province (11) based on their rDNA-ITS2Manuscript sequences and also investigated the utility of this fragment in the phylogeny of the six studied species and phylogeography of the medically important species Anopheles maculipennis. 3 Material and methods Study area, sample collection and morphological identification All samples were collected from the West Azerbaijan Province, Iran (Table 1). Mosquitoes were collected monthly from May to November 2012. Larvae were collected using a standard dipping method. For collecting adult mosquitoes, several methods were used such as hand catches, night landing catches on cows, pit shelter collection, and total catch (a human or animal dwelling was cowered by white cottons and all entrances and exits of the location were closed before spraying insecticides for less than one minute. After 10-15 minutes all windows and doors were opened and the white cotton textures carefully inspected for dead or knocked-down mosquitoes). All samples were identified to the species level using a standard morphological key (12) and the accurate morphological identification was confirmed with PCR for 2-3 specimens of each species. Genomic DNA extraction and ITS2 fragment amplification Nine populations of six species were subjected to molecular analysis. The genomic DNA of mosquitoes was extracted by Bioneer AccuPrep® Genomic DNA Extraction Kit (South Korea) according to the manufacturer’s instructions. Extracted DNA was diluted in TE buffer and kept at 4 °C. The desired ITS2 fragments were amplified using as forward primer universal 5.8S (5' ATC ACT CGG CTC GTG GAT CG 3') and as reverse primer universal 28S (5' ATG CTT AAA TTT AGG GGG TAG TC 3') (13). The PCR conditions were 94°C for 5 min followed by 30 cycles of [94°CAccepted for 45 s, 57°C for 50 s, 72°C for Manuscript 1 min] and 72°C for 10 min. The accuracy and quality of amplicons were examined on a 1.5% agarose gel and visualized by UV transillumination after staining with CinnaGen® safe stain (Iran). High quality amplicons of the desired size were sequenced. 4 Phylogenetic analysis For phylogenetic analysis, ITS2 sequences from the same mosquito species were retrieved from GenBank when available (www.ncbi.nlm.nih.gov). The evolutionary history was inferred by using the Maximum Likelihood method based on the Tamura-Nei model (14). Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood (MCL) approach, and then selecting the topology with superior log likelihood value. A discrete Gamma distribution was used to model evolutionary rate differences among sites (5 categories (+G, parameter = 8.9461)). All positions containing gaps and missing data were eliminated. There were a total of 193 positions in the final dataset. Evolutionary analyses were conducted in MEGA6 (15). Results In this study, nine populations of six species of mosquitoes were investigated including both subfamilies Anophelinae and Culicinae, from the West Azerbaijan Province in northwestern Iran. The rDNA ITS2 region was successfully amplified and sequenced for a representative subset of the six species (Table 1). Three populations from north, centre and south of West Azerbaijan Province of Anopheles maculipennis (Subfamily Anophelinae, Genus Anopheles, Subgenus Anopheles), two populations of An. superpictus (Subfamily Anophelinae, Genus Anopheles, Subgenus Cellia), Culex hortensis (SubfamilyAccepted Culicinae, Genus Culex, SubgenusManuscript Maillotia), Culex theileri (Subfamily Culicinae, Genus Culex, Subgenus Culex), Culiseta longiareolata (Subfamily Culicinae, Genus 5 Culiseta, Subgenus Allotheobaldia) and Ochlerotatus caspius (Subfamily Culicinae, Genus Ochlerotatus, Subgenus Ochlerotatus). The Phylogenetic analysis based on the amplified fragment showed that the ITS2 sequences of studied species could successfully differentiate the different taxonomic levels including the members of Subfamilies Anophelinae and Culicinae, different genera ( Anopheles, Culex, Culiseta and Ochlerotatus) (Fig. 1). About the different populations of the An. maculipennis (three populations from different geographical regions of study area) and An. superpictus (two populations from wetland and mountainous areas), it seems that using the ITS2 fragment could differ the mentioned populations as well. Regarding the presence of An. maculipennis complex in this region, the acquired sequences of three different populations of this species in this study (KF483845, KF483842 and KF483834) and some of other sequences of ITS2 fragment of this species from other regions (FJ210887
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