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Development of a multiplex PCR assay for the identification of eight species members of the Thai Hyrcanus Group (Diptera: Culicidae)

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Abstract

The Hyrcanus Group comprises important vectors of malaria because of Plasmodium vivax Grassi and Feletti and filariasis caused by Brugia malayi Brug in many countries of South, Southeast and East Asian regions. In Thailand, eight species members (Anopheles argyropus Swellengrebel, An. crawfordi Reid, An. nigerrimus Giles, An. nitidus Harrison, Scanlon & Reid, An. paraliae Sandosham, An. peditaeniatus Leicester, An. pursati Laveran and An. sinensis Wiedemann) of the Hyrcanus Group have been recognized. Due to morphological overlap, adult females of the Hyrcanus Group in Thailand have been misidentified markedly among the eight species, particularly when using the traumatic scales of wild-caught specimens from epidemiology and control approaches. Therefore, this study first developed a simple and robust multiplex PCR assay, based on second internal transcribed spacer sequences of ribosomal DNA, for differentiating the eight species members of the Thai Hyrcanus Group.

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References

  • Alam MS, Khan MG, Chaudhury N, Deloer S, Nazib F, Bangali AM, Haque R (2010) Prevalence of anopheline species and their Plasmodium infection status in epidemic-prone border areas of Bangladesh. Malar J 9:15

    Article  PubMed  Google Scholar 

  • Alam MS, Chakma S, Khan WA, Glass GE, Mohon AN, Elahi R, Norris LC, Podder MP, Ahmed S, Haque R, Sack DA, Sullivan DJ Jr, Norris DE (2012) Diversity of anopheline species and their Plasmodium infection status in rural Bandarban, Bangladesh. Parasit Vectors 5:150

    Article  CAS  Google Scholar 

  • Baker EZ, Beier JC, Meek SR, Wirtz RA (1987) Detection and quantification of Plasmodium falciparum and P. vivax infections in Thai-Kampuchean Anopheles (Diptera: Culicidae) by enzyme-linked immunosorbent assay. J Med Entomol 24:537–541

    Google Scholar 

  • Beebe NW, Saul A (1995) Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction-restriction fragment length polymorphism analysis. Am J Trop Med Hyg 53:478–481

    PubMed  CAS  Google Scholar 

  • Chai JY (1999) Re-emerging Plasmodium vivax malaria in the Republic of Korea. Korean J Parasitol 37:129–143

    Article  PubMed  CAS  Google Scholar 

  • Choi KS, Townson H (2012) Evidence for X-linked introgression between molecular forms of Anopheles gambiae from Angola. Med Vet Entomol 26:218–227

    Article  PubMed  CAS  Google Scholar 

  • Choochote W (2011) Evidence to support karyotypic variation of the mosquito, Anopheles peditaeniatus in Thailand. J Insect Sci 11:10

    Article  PubMed  Google Scholar 

  • Djadid ND, Jazayeri H, Gholizadeh S, Rad SP, Zakeri S (2009) First record of a new member of Anopheles hyrcanus group from Iran: molecular identification, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Entomol 46:1084–1093

    Article  PubMed  Google Scholar 

  • Foley DH, Paru R, Dagoro H, Bryan JH (1993) Allozyme analysis reveals six species within the An. punctulatus complex of mosquitoes in Papua New Guinea. Med Vet Entomol 7:37–48

    Article  PubMed  CAS  Google Scholar 

  • Frances SP, Klein TA, Wirtz RA, Eamsila C, Pilakasiri C, Linthicum KJ (1996) Plasmodium falciparum and P. vivax circumsporozoite proteins in anophelines (Diptera: Culicidae) collected in eastern Thailand. J Med Entomol 33:990–991

    PubMed  CAS  Google Scholar 

  • Garros C, Koekemoer LL, Coetzee M, Coosemans M, Manguin S (2004) A single multiplex assay to identify major malaria vectors within the African Anopheles funestus and the Oriental An. minimus groups. Am J Trop Med Hyg 70:583–590

    PubMed  CAS  Google Scholar 

  • Gingrich JB, Weatherhead A, Sattabongkot J, Pilakasiri C, Wirtz RA (1990) Hyperendemic malaria in Thai Village: dependence of year-round transmission on focal and seasonally circumscribed mosquito (Diptera: Culicidae) habitats. J Med Entomol 27:1016–1026

    PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

  • Harbach RE (2013) Anopheles classification. Mosquito taxonomic inventory. http://mosquito-taxonomic-inventory.info/anophelesclassification. Accessed 10 May 2013

  • Harbach RE, Gingrich JB, Pang LW (1987) Some entomological observations on malaria transmission in a remote village in northwestern Thailand. J Am Mosq Control Assoc 3:296–301

    PubMed  CAS  Google Scholar 

  • Harrison BA, Scanlon JE (1975) Medical entomology studies II. The subgenus Anopheles in Thailand (Diptera: Culicidae). Contrib Am Entomol Inst 12:1–307

    Google Scholar 

  • Henry-Halldin CN, Reimer L, Thomsen E, Koimbu G, Zimmerman A, Keven JB, Dagoro H, Hetzel MW, Mueller I, Siba P, Zimmerman PA (2011) High throughput multiplex assay for species identification of Papua New Guinea malaria vectors: members of the Anopheles punctulatus (Diptera: Culicidae) species group. Am J Trop Med Hyg 84:166–173

    Article  PubMed  CAS  Google Scholar 

  • Joshi D, Park MH, Saeung A, Choochote W, Min GS (2010) Multiplex assay to identify Korean vectors of malaria. Mol Ecol Resour 10:748–750

    Article  PubMed  CAS  Google Scholar 

  • Kanojia PC, Shetty PS, Geevarghese G (2003) A long-term study on vector abundance & seasonal prevalence in relation to the occurrence of Japanese encephalitis in Gorakhpur district, Uttar Pradesh. Indian J Med Res 117:104–110

    PubMed  CAS  Google Scholar 

  • Kimura M (1980) Simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wilkerson RC (2007) Intragenomic rDNA ITS2 variation in the neotropical Anopheles (Nyssorhynchus) albitarsis complex (Diptera: Culicidae). J Hered 98:51–59

    Article  PubMed  CAS  Google Scholar 

  • Li C, Lee JS, Groebner JL, Kim HC, Klein TA, O’Guinn ML, Wilkerson RC (2005) A newly recognized species in the Anopheles Hyrcanus Group and molecular identification of related species from the Republic of South Korea (Diptera: Culicidae). Zootaxa 939:1–8

    Google Scholar 

  • Liu C (1990) Comparative studies on the role of Anopheles anthropophagus and Anopheles sinensis in malaria transmission in China. Zhonghua Liu Xing Bing Xue Za Zhi 11:360-363

    PubMed  CAS  Google Scholar 

  • Manguin S, Bangs MJ, Pothikasikorn J, Chareonviriyaphap T (2010) Review on global co-transmission of human Plasmodium species and Wuchereria bancrofti by Anopheles mosquitoes. Infect Genet Evol 10:159–177

    Article  PubMed  CAS  Google Scholar 

  • Min GS, Choochote W, Jitpakdi A, Kim SJ, Kim W, Jung J, Junkum A (2002) Intraspecific hybridization of Anopheles sinensis (Diptera: Culicidae) strains from Thailand and Korea. Mol Cells 14:198–204

    PubMed  CAS  Google Scholar 

  • Mourya DT, Ilkal MA, Mishra AC, Jacob PG, Pant U, Ramanujam S, Mavale MS, Bhat HR, Dhanda V (1989) Isolation of Japanese encephalitis virus from mosquitoes collected in Karnataka State, India from 1985 to 1987. Trans R Soc Trop Med Hyg 83:550–552

    Article  PubMed  CAS  Google Scholar 

  • Norris DE (2002) Genetic markers for study of the anopheline vectors of human malaria. Int J Parasitol 32:1607–1615

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

    Google Scholar 

  • Paredes-Esquivel C, Donnelly MJ, Harbach RE, Townson H (2009) A molecular phylogeny of mosquitoes in the Anopheles barbirostris subgroup reveals cryptic species: implications for identification of disease vectors. Mol Phylogenet Evol 50:141–151

    Article  PubMed  CAS  Google Scholar 

  • Paredes-Esquivel C, Harbach RE, Townson H (2011) Molecular taxonomy of members of the Anopheles hyrcanus group from Thailand and Indonesia. Med Vet Entomol 25:348–352

    Article  PubMed  CAS  Google Scholar 

  • Park SJ, Choochote W, Jitpakdi A, Junkum A, Kim SJ, Jariyapan N (2003) Evidence for a conspecific relationship between two morphologically and cytologically different Forms of Korean Anopheles pullus mosquito. Mol Cells 16:354–360

    PubMed  CAS  Google Scholar 

  • Phuc HK, Ball AJ, Son L, Hanh NV, Tu ND, Lien NG, Verardi A, Townson H (2003) Multiplex PCR assay for malaria vector Anopheles minimus and four related species in the Myzomyia Series from Southeast Asia. Med Vet Entomol 17:423–428

    Article  PubMed  CAS  Google Scholar 

  • Raghavendra K, Cornel AJ, Reddy BP, Collins FH, Nanda N, Chandra D, Verma V, Dash AP, Subbarao SK (2009) Multiplex PCR assay and phylogenetic analysis of sequences derived from D2 domain of 28S rDNA distinguished members of the Anopheles culicifacies complex into two groups, A/D and B/C/E. Infect Genet Evol 9:271–277

    Article  PubMed  CAS  Google Scholar 

  • Rattanarithikul R, Konishi E, Linthicum KJ (1996) Detection of Plasmodium vivax and Plasmodium falciparum circumsporozoites antigen in anopheline mosquitoes collected in southern Thailand. Am J Trop Med Hyg 54:114–121

    PubMed  CAS  Google Scholar 

  • Rattanarithikul R, Harrison BA, Harbach RE, Panthusiri P, Coleman RE (2006) Illustrated keys to the mosquitoes of Thailand IV. Anopheles. Southeast Asian J Trop Med Public Health 37(suppl 2):1–128

    Google Scholar 

  • Ree HI, Hwang UW, Lee IY, Kim TE (2001) Daily survival and human blood index of Anopheles sinensis, the vector species of malaria in Korea. J Am Mosq Control Assoc 17:67–72

    PubMed  CAS  Google Scholar 

  • Reid JA (1953) The Anopheles hyrcanus group in South-East Asia (Diptera: Culicidae). Bull Ent Res 44:5-76

    Article  Google Scholar 

  • Reid JA (1968) Anopheline mosquitoes of Malaya and Borneo. Stud Inst Med Res Malaysia 31:1–520

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Saeung A, Baimai V, Thongsahuan S, Min GS, Park MH, Otsuka Y, Maleewong W, Lulitanond V, Taai K, Choochote W (2012) Geographic distribution and genetic compatibility among six karyotypic forms of Anopheles peditaeniatus (Diptera: Culicidae) in Thailand. Trop Biomed 29:613–625

    PubMed  CAS  Google Scholar 

  • Saeung A, Hempolchom C, Baimai V, Thongsahuan S, Taai K, Jariyapan N, Chaithong U, Choochote W (2013) Susceptibility of eight species members of Anopheles hyrcanus group to nocturnally subperiodic Brugia malayi. Parasit Vectors 6:5

    Article  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Scanlon JE, Peyton EL, Gould DJ (1968) An annotated checklist of the Anopheles of Thailand. Thai Natl Sci Pap Fauna Ser 2:1–35

    Google Scholar 

  • Swain S, Mohanty A, Mahapatra N, Parida SK, Marai NS, Tripathy HK, Kar SK, Hazra RK (2009) The development and evaluation of a single step multiplex PCR for simultaneous detection of Anopheles annularis group mosquitoes, human host preference and Plasmodium falciparum sporozoite presence. Trans R Soc Trop Med Hyg 103:1146–1152

    Article  PubMed  CAS  Google Scholar 

  • Taai K, Baimai V, Saeung A, Thongsahuan S, Min GS, Otsuka Y, Park MH, Fukuda M, Somboon P, Choochote W (2013) Genetic compatibility between Anopheles lesteri from Korea and Anopheles paraliae from Thailand. Mem Inst Oswaldo Cruz 108:312–320

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolution genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Whang IJ, Jung J, Park JK, Min GS, Kim W (2002) Intragenomic length variation of the ribosomal DNA intergenic spacer in a malaria vector, Anopheles sinensis. Mol Cells 14:158–162

    PubMed  CAS  Google Scholar 

  • Wilkerson RC, Cong L, Rueda LM, Kim HC, Klein TA, Song GH, Strickman D (2003) Molecular confirmation of Anopheles (Anopheles) lesteri from the Republic of South Korea and its genetic identity with An. anthropophagus from China (Diptera: Culicidae) Zootaxa 378:1–14

    Google Scholar 

  • Zhang HL (1990) The natural infection rate of mosquitoes by Japanese encephalitis B virus in Yunnan Province. Zhonghua Yu Fang Yi Xue Za Zhi 24:265–267

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Thailand Research Fund (TRF Senior Research Scholar: RTA5480006) and the Diamond Research Grant of the Faculty of Medicine, Chiang Mai University, to W. Choochote and A. Saeung. The authors would like to thank Dr. Wattana Navacharoen, Dean of the Faculty of Medicine, Chiang Mai University, for his interest in this research.

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Correspondence to Wej Choochote.

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Hempolchom, C., Otsuka, Y., Baimai, V. et al. Development of a multiplex PCR assay for the identification of eight species members of the Thai Hyrcanus Group (Diptera: Culicidae). Appl Entomol Zool 48, 469–476 (2013). https://doi.org/10.1007/s13355-013-0207-1

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