Molecular identification and phylogenetic analysis of Pulex irritans in different regions of Iran

Document Type : Research Article

Authors

Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, West Azerbaijan, Iran.

Abstract

The present study was conducted to perform a molecular comparison of Pulex irritans based on the mitochondrial genome in four different climatic regions including the Caspian Sea region, a mountainous region, Persian Gulf region,  and the Central Desert region, and based on nuclear ribosome genome in the west and northwestern Iran. A total of 1937 adult flea samples were collected including 1019 P. irritans (52.61%) and 918 Ctenocephalides canis (47.39%) from various hosts including humans (14.1%), sheep (22%), goats (33.5%), dogs (25.6%) and houses (6.7%) between April 2018 and May 2019. The samples collected from different hosts had similar morphological characteristics. However, there were slight differences based on mitochondrial markers and nuclear ribosomal markers in the study populations. The results from the phylogenetic tree based on three nuclear ribosome and mitochondrial markers showed that despite the slight differences in this sequence of different hosts and cities, all samples from different regions are in the same phylogeny. The results of ribosomal and mitochondrial genome analysis showed that these pieces are useful for demonstrating intraspecific similarity, and differentiation at species level and genus of P. irritans.

Keywords

Main Subjects


1.    Lewis RE. Resume of the Siphonaptera (Insecta) of the world. J Med Entom. 1998; 1; 35(4): 377-389.
2.    Azizi MH, Azizi F. A history of the human plague in Iran. Arch Iran Med. 2010; 13(6): 563-569.
3.    Esamaeili S, Azadmanesh K, Naddaf SR, Rajerison M, Carniel E, Mostafavi E. Serologic survey of plague in animals, Western Iran. Emerg Infec Dis. 2013; 19(9):1549.
4.    Tavassoli M, Ahmadi A, Imani A, Ahmadiara E, Javadi S, Hadian M. Survey of flea infestation in dogs in different geographical regions of Iran. Korean J parasitol. 2010; 48(2):145.
5.    Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D. Fleas and flea-borne diseases. In J Infec Dis. 2010;14(8): 667-676.
6.    Leulmi H, Socolovschi C, Laudisoit A, Houemenou G, Davoust B, Bitam I, Raoult D, Parola P. Detection of Rickettsia felis, Rickettsia typhi, Bartonella species and Yersinia pestis in fleas (Siphonaptera) from Africa. PLoS Negl Trop Dis. 2014; 8(10): 3152.
7.    Ratovonjato J, Rajerison M, Rahelinirina S, Boyer S. Yersinia pestis in Pulex irritans fleas during plague outbreak, Madagascar. Emerg Infect Dis. 2014; 20(8):e1414.
8.    Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L. Plague: past, present, and future. PLoS Med. 2008; 5(1):e3152.
9.    Azarm A, Dalimi A, Mohebali M, Mohammadiha A, Zarei Z. Morphological and molecular characterization of Ctenocephalides spp isolated from dogs in north of Iran. J Entomol. 2016; 4(4):713-717.
10.    Gamerschlag S, Mehlhorn H, Heukelbach J, Feldmeier H, D’Haese J. Repetitive sequences in the ITS1 region of the ribosomal DNA of Tunga penetrans and other flea species (Insecta, Siphonaptera). Parasito Res. 2008; 102(2): 193-199.
11.    Vobis M, D’Haese J, Mehlhorn H, Mencke N, Blagburn BL, Bond R, Denholm I, Dryden MW, Payne P, Rust MK, Schroeder I. Molecular phylogeny of isolates of Ctenocephalides felis and related species based on analysis of ITS1, ITS2 and mitochondrial 16S rDNA sequences and random binding primers. Parasitol Res. 2004; 94(3): 219-226
12.    Zurita A, Callejon R, Garcia‐sanchez ÁM, Urdapilleta M, Lareschi M, Cutillas C. Origin, evolution, phylogeny and taxonomy of Pulex irritans. Med Vet Entomol. 2019; 33(2): 296-311.
13.    Bowen BW, Clark AM, Abreu-Grobois FA, Chaves A, Reichart HA, Ferl RJ. Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica. 1997; 101(3): 179-189.
14.    Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 1994; 87(6): 651-701.
15.    Mclain DK, Wesson DM, Oliver Jr JH, Collins FH. Variation in ribosomal DNA internal transcribed spacers 1 among eastern populations of Ixodes scapularis (Acari: Ixodidae). J Med Entomol. 1995; 32(3):353-560.
16.    Lv J, Wu S, Zhang Y, Chen Y, Feng C, Yuan X, Jia G, Deng J, Wang C, Wang Q, Mei L. Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida). Parasites  vectors. 2014; 7(1):1-1.
17.    Bahrami S, Kharrati L, Makki M. The First Case Report of Human Infestation with Ctenocephalides canis in Behbahan (Khuzestan Province). J of Ardabil Univ of Med Sci. 2016; 16(3): 317-322.
18.    Yakhchali M, Hosseine A. Prevalence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Vet Arhiv. 2006; 76(5): 431-442.
19.    Van der Mescht L, Matthee S, Matthee CA. Comparative phylogeography between two generalist flea species reveal a complex interaction between parasite life history and host vicariance: parasite-host association matters. BMC Evol Biol. 2015; 15(1):1-5.
20.    Hornok S, Beck R, Farkas R, Grima A, Otranto D, Kontschan J, Takacs N, Horváth G, Szoke K, Szekeres S, Majoros G. High mitochondrial sequence divergence in synanthropic flea species (Insecta: Siphonaptera) from Europe and the Mediterranean. Parasites  vectors. 2018; 11(1):1-1.
21.    Seyyed‐Zadeh SJ, Bozorg‐Omid F, Telmadarraiy Z, Terenius O, Chavshin AR. Evidence for the presence of Ctenocephalides orientis in livestock dwellings in northwest Iran. Med Vet Entomol. 2018; 32(3): 383-387.
22.    Zurita A, Callejon R, De Rojas M, Halajian A, Cutillas C. Ctenocephalides felis and Ctenocephalides canis: introgressive hybridization?. Syst Entomol. 2016; 41(3): 567-579.
23.    Krasnov BR, Shenbrot GI, Khokhlova IS. Historical biogeography of fleas: the former Bering Land Bridge and phylogenetic dissimilarity between the Nearctic and Palearctic assemblages. Parasitol Res. 2015; 114(5): 1677-1686.
24.    Marrugal A, Callejón R, de Rojas M, Halajian A, Cutillas C. Morphological, biometrical, and molecular characterization of Ctenocephalides felis and Ctenocephalides canis isolated from dogs from different geographical regions. Parasitol Res. 2013; 112(6): 2289-2298.
25.    Ghavami MB, Mirzadeh H, Mohammadi J, Fazaeli A. Molecular survey of ITS1 spacer and Rickettsia infection in human flea, Pulex irritans. Parasitol Res. 2018; 117(5):1433-1442.
26.    Skerman KD, Shahlapoor AA, Eslami AH, Eliazian M. Observations on the incidence, epidemiology, control and economic importance of gastro-intestinal parasites of sheep and goats in Iran. Arch Razi Inst. 1970; 22(1): 187-196.
27.    Asmar M, Piazak N, Karimi Y. An illustrated key for flea of Iran: Pasteur Institute of Iran, Tehran (Persian), 1979; 2-15. 
28.    Shayan A, Rafinejad J. Arthropod parasites of rodents in Khorram Abbad district, Lorestan Provincen of Iran. Iranian J Public Health. 2006; 70-6.
29.    Lawrence AL, Hii SF, Jirsova D, Panakova L. Integrated morphological and molecular identification of cat fleas (Ctenocephalides felis) and dog fleas (Ctenocephalides canis) vectoring Rickettsia felisin central Europe. Vet Parasitol. 2015; 10(3-4): 215–23. 
30. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoeket R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Ma Biol Biotechnol. 1994; 3(5): 294–299.