Genetic differentiation between sandfly populations of Phlebotomus chinensis and Phlebotomus sichuanensis (Diptera: Psychodidae) in China inferred by microsatellites
Tóm tắt
Phlebotomus chinensis is a primary vector of visceral leishmaniasis; it occurs in various biotopes with a large geographical distribution, ranging from Yangtze River to northeast China. Phlebotomus sichuanensis, a species closely related to P. chinensis in high altitude regions, has a long term disputation on its taxonomic status. Both species occur in the current epidemic regions and are responsible for the transmission of leishmaniasis. Population genetic analysis will help to understand the population structure and infer the relationship for morphologically indistinguishable cryptic species. In this study, microsatellite markers were used for studying the genetic differentiation between P. chinensis and P. sichuanensis. Sandflies were collected in 6 representative localities in China in 2005-2009. Ten microsatellite loci were used to estimate population genetic diversity. The intra-population genetic diversity, genetic differentiation and effective population size were estimated. All 10 microsatellite loci were highly polymorphic across populations, with high allelic richness and heterozygosity. Hardy-Weinberg disequilibrium was found in 23 out of 60 (38.33%) comparisons associated with heterozygote deficits, which was likely caused by the presence of null allele and the Wahlund effect. Bayesian clustering analysis revealed three clusters. The cluster I included almost all specimens in the sample SCD collected at high altitude habitats in Sichuan. The other two clusters were shared by the remaining 5 populations, SCJ in Sichuan, GSZ in Gansu, SXL and SXX in Shaanxi and HNS in Henan. The diversity among these 5 populations was low (FST = -0.003-0.090) and no isolation by distance was detected. AMOVA analysis suggested that the variations were largely derived from individuals within populations and among individuals. Consistently, the analysis of ribosomal DNA second internal transcribed spacer (ITS2) sequence uncovered three types of variants, which corresponded with the three gene pools revealed by microsatellites. The data suggested that the SCD population carried a distinct gene pool, which was differentiated from the other populations. The high altitude ecological habitats, distinctive ITS2 and herein divergence inferred by microsatellite loci support the species status of P. sichuanensis. The P. chinensis populations did not have a significant divergence from each another.
Tài liệu tham khảo
Leng YJ, Zhang LM: Check list and geographical distribution of phlebotomine sandflies in China. Ann Trop Med Parasitol. 1993, 87 (1): 83-94.
Zhang LM, Leng YJ: Eighty-year research of phlebotomine sandflies (Diptera: Psychodidae) in China (1915-1995). II. Phlebotomine vectors of leishmaniasis in China. Parasite. 1997, 4 (4): 299-306.
Wang JY, Cui G, Chen HT, Zhou XN, Gao CH, Yang YT: Current epidemiological profile and features of visceral leishmaniasis in People’s Republic of China. Parasit Vectors. 2012, 5: 31-10.1186/1756-3305-5-31.
Guan LR, Shen WX: Recent advances in visceral leishmaniasis in China. Southeast Asian J Trop Med Public Health. 1991, 22 (3): 291-298.
Leng YJ, Yin ZC: The taxonomy of phlebotomine sandflies (Diptera: Psychodidae) of Sichuan Province, China, with descriptions of two species, Phlebotomus (Adlerius) sichuanensis sp. n. and Sergentomyia (Neophlebotomus) zhengjiani sp. n. Ann Trop Med Parasitol. 1983, 77 (4): 421-431.
Leng YJ, Zhang LM: Chinese phlebotomine sandflies of subgenus Adlerius nitzulescu,(Diptera: Psychodidae) and the identity of Phlebotomus sichuanensis Leng & Yin, 1983. Part I-Taxonomical study and geographical distribution. Parasite. 1931, 8 (1): 3-9.
Leng YJ, Zhang LM, Zhang BX: A study of phlebotomine sandflies (Diptera: Psychodidae) in Yunnan Province, China. I. Phlebotomine sandflies of northeastern and western Yunnan. Parassitologia. 1991, 33 (Suppl): 373-375.
Xiong GH, Jin CF, Hong YM: Further study on the type of sandfly Ph. chinensis in southern Gansu and Northern Sichuan. Endemic Dis Bull. 1990, 5: 53-60.
Xiong GH, Jin CF: Studies on the longitudinal distribution of sandfly Phlebotomus chinensis and its relation to Kala Azar in southern Gansu and northern Sichuan. Endemic Diseases Bulletin. 1989, 4 (4): 15-21.
Latrofa MS, Annoscia G, Dantas-Torres F, Traversa D, Otranto D: Towards a rapid molecular identification of the common phlebotomine sand flies in the Mediterranean region. Vet Parasitol. 2012, 184 (2–4): 267-270.
Kumar NP, Srinivasan R, Jambulingam P: DNA barcoding for identification of sand flies (Diptera: Psychodidae) in India. Mol Ecol Resour. 2012, 12 (3): 414-420. 10.1111/j.1755-0998.2012.03117.x.
Khalid N, Elnaiem D, Aboud M, Al Rabba F, Tripet F: Morphometric and molecular differentiation of Phlebotomus (Phlebotomus) sandflies. Med Vet Entomol. 2010, 4 (4): 352-360.
Depaquit J, Naucke TJ, Schmitt C, Ferte H, Leger N: A molecular analysis of the subgenus Transphlebotomus Artemiev, 1984 (Phlebotomus, Diptera, Psychodidae) inferred from ND4 mtDNA with new northern records of Phlebotomus mascittii Grassi, 1908. Parasitol Res. 2005, 95 (2): 113-116. 10.1007/s00436-004-1254-x.
Depaquit J, Ferte H, Leger N, Lefranc F, Alves-Pires C, Hanafi H, Maroli M, Morillas-Marquez F, Rioux JA, Svobodova M: ITS2 sequences heterogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodidae): possible consequences in their ability to transmit Leishmania tropica. Int J Parasitol. 2002, 32 (9): 1123-1131. 10.1016/S0020-7519(02)00088-7.
Depaquit J, Ferte H, Leger N, Killick-Kendrick R, Rioux JA, Killick-Kendrick M, Hanafi HA, Gobert S: Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses of dispersion and speciation. Insect Mol Biol. 2000, 9 (3): 293-300. 10.1046/j.1365-2583.2000.00179.x.
Di Muccio T, Marinucci M, Frusteri L, Maroli M, Pesson B, Gramiccia M: Phylogenetic analysis of Phlebotomus species belonging to the subgenus Larroussius (Diptera, psychodidae) by ITS2 rDNA sequences. Insect Biochem Mol Biol. 2000, 30 (5): 387-393. 10.1016/S0965-1748(00)00012-6.
Belen A, Kucukyildirim S, Alten B: Genetic structures of sand fly (Diptera: Psychodidae) populations in a leishmaniasis endemic region of Turkey. J Vector Ecol. 2011, 36 (Suppl 1): S32-S48.
Hamarsheh O, Presber W, Yaghoobi-Ershadi MR, Amro A, Al-Jawabreh A, Sawalha S, Al-Lahem A, Das ML, Guernaoui S, Seridi N: Population structure and geographical subdivision of the Leishmania major vector Phlebotomus papatasi as revealed by microsatellite variation. Med Vet Entomol. 2009, 23 (1): 69-77. 10.1111/j.1365-2915.2008.00784.x.
Hamarsheh O, Presber W, Al-Jawabreh A, Abdeen Z, Amro A, Schonian G: Molecular markers for Phlebotomus papatasi (Diptera: Psychodidae) and their usefulness for population genetic analysis. Trans R Soc Trop Med Hyg. 2009, 103 (11): 1085-1086. 10.1016/j.trstmh.2009.02.011.
Depaquit J, Lienard E, Verzeaux-Griffon A, Ferte H, Bounamous A, Gantier JC, Hanafi HA, Jacobson RL, Maroli M, Moin-Vaziri V: Molecular homogeneity in diverse geographical populations of Phlebotomus papatasi (Diptera, Psychodidae) inferred from ND4 mtDNA and ITS2 rDNA epidemiological consequences. Infect Genet Evol. 2008, 8 (2): 159-170. 10.1016/j.meegid.2007.12.001.
Hamarsheh O, Presber W, Abdeen Z, Sawalha S, Al-Lahem A, Schonian G: Genetic structure of mediterranean populations of the sandfly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis. Med Vet Entomol. 2007, 21 (3): 270-277. 10.1111/j.1365-2915.2007.00695.x.
Hamarsheh O, Amro A: Characterization of simple sequence repeats (SSRs) from Phlebotomus papatasi (Diptera: Psychodidae) expressed sequence tags (ESTs). Parasit Vectors. 2011, 4: 189-10.1186/1756-3305-4-189.
Aransay AM, Ready PD, Morillas-Marquez F: Population differentiation of Phlebotomus perniciosus in Spain following postglacial dispersal. Heredity (Edinb). 2003, 90 (4): 316-325. 10.1038/sj.hdy.6800246.
Mahamdallie SS, Pesson B, Ready PD: Multiple genetic divergences and population expansions of a Mediterranean sandfly, Phlebotomus ariasi, in Europe during the Pleistocene glacial cycles. Heredity (Edinb). 2011, 106 (5): 714-726. 10.1038/hdy.2010.111.
Zhang L, Ma Y: Identification of Phlebotomus chinensis (Diptera: Psychodidae) inferred by morphological characters and molecular markers. Entomotaxonomia. 2012, 34 (1): 71-80.
Lu B, Wu H: Classification and identification of important medical insects of China. 2003, Henan: Henan Science and Technology Publishing House
Zhang L, Ma Y: Isolation of microsatellite DNA and the polymorphic locus screening from Phlebotomus chinensis. Chin J Parasitol Parasit Dis. 2009, 27 (6): 503-507.
Schuelke M: An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol. 2000, 18 (2): 233-234. 10.1038/72708.
Nei M: Molecular evolutionary genetics. 1987, New York: Colombia University Press
Goudet J: FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered. 1995, 86 (6): 485-486.
Brookfield JF: A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol. 1996, 5 (3): 453-455.
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004, 4 (3): 535-538. 10.1111/j.1471-8286.2004.00684.x.
Raymond M, Rousset F: GENEPOP (Version 1.2): Population genetics software for exact tests and ecumenicism. J Hered. 1995, 86 (3): 248-249.
Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005, 14 (8): 2611-2620. 10.1111/j.1365-294X.2005.02553.x.
Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155 (2): 945-959.
Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online. 2005, 1: 47-50.
Slatkin M: A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995, 139 (1): 457-462.
Gaggiotti OE, Lange O, Rassmann K, Gliddon C: A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol. 1999, 8 (9): 1513-1520. 10.1046/j.1365-294x.1999.00730.x.
Mantel N: The detection of disease clustering and a generalized regression approach. Cancer Res. 1967, 27 (2): 209-220.
Ovenden JR, Peel D, Street R, Courtney AJ, Hoyle SD, Peel SL, Podlich H: The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol. 2007, 16 (1): 127-138.
Wang ZJ, Xiong GH, Guan LR: The achievement of Leishmaniasis control in China. Chin J Epidem. 2000, 21 (1): 51-54.
Guan LR, Wang J, Liu PZ, Chang ZG: The Bionomics of Phleboomus chinensis in the nountainous regions of southern Kansu and the Loess Plateau of northern Shensi. Acta Entomol Sin. 1980, 23 (1): 25-31.
Della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, Petrarca V, Coluzzi M: Molecular evidence of incipient speciation within Anopheles gambiae s. s. in West Africa. Insect Mol Biol. 2001, 10 (1): 9-18. 10.1046/j.1365-2583.2001.00235.x.
Gentile G, Slotman M, Ketmaier V, Powell JR, Caccone A: Attempts to molecularly distinguish cryptic taxa in Anopheles gambiae s. s. Insect Mol Biol. 2001, 10 (1): 25-32. 10.1046/j.1365-2583.2001.00237.x.
Lawniczak MK, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, Redmond S, Fulton L, Appelbaum E, Godfrey J: Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science. 2010, 330 (6003): 512-514. 10.1126/science.1195755.
Ma Y, Bu L, Hua X: [20-year search on molecular markers of Leishmania isolates from different Kala-azar foci in China to confirm whether genetic fingerprints of Kala-azar pathogens correlate with disease types]. J Biomed Engineer. 2011, 28 (5): 997-1000.