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Host-specific Wolbachia strains in widespread populations of Phlebotomus perniciosus and P. papatasi (Diptera: Psychodidae), and prospects for driving genes into these vectors of Leishmania

Published online by Cambridge University Press:  09 March 2007

M. Benlarbi
Affiliation:
Molecular Systematics Laboratory, Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
P.D. Ready*
Affiliation:
Molecular Systematics Laboratory, Department of Entomology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
*
*Fax: +44 (0)20 7942 5229 E-mail: P.Ready@nhm.ac.uk

Abstract

A single strain of Wolbachia (α-proteobacteria, Rickettsiales) was found in widespread geographical populations of each of two Phlebotomus species, within which there was no indication of ‘infectious speciation’. The two strains were identified by sequencing a fragment of wsp (a major surface protein gene), amplified by polymerase chain reaction from DNA extracted from the body parts of individual sandflies. Infection rates were high in the males and females of both sandflies, but they were lower for the B-group wPrn strain of Wolbachia in Phlebotomus perniciosus Newstead (60.3% overall) than for the A-group wPap strain in P. papatasi (Scopoli) (81.7%). Infections were frequent in the thorax, where Leishmania develops infective forms, as well as in the abdomen, where Wolbachia must infect the reproductive tissues to ensure its vertical transmission. These findings were related to knowledge of the population biology of Wolbachia in other insects, leading to the conclusion that this endosymbiont could be useful for driving transgenes through wild populations of both sandflies. This will require characterizing the cytoplasmic incompatibility phenotypes of Wolbachia–sandfly combinations, as well as estimating for them the incidence of paternal transmission and the fidelity of maternal transmission. Paternal transmission is one explanation for finding a single Wolbachia strain associated with all mitochondrial haplotypes and lineages of each sandfly species. However, this distribution pattern could also result from multiple horizontal transmissions or the failure of wsp to provide strain markers.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2003

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References

Aransay, A.M., Malarky, G. & Ready, P.D. (2001) Isolation (with enrichment) and characterization of trinucleotide microsatellites from Phlebotomus perniciosus, a vector of Leishmania infantum. Molecular Ecology Notes 1, 176178.CrossRefGoogle Scholar
Aransay, A.M., Ready, P.D. & Morillas-Marquez, F. (2003) Population differentiation of Phlebotomus perniciosus in Spain following post-glacial dispersal. Heredity 90, 316325.CrossRefGoogle Scholar
Ashford, R.W., Desjeux, P. & De Raadt, P. (1992) Estimation of population at risk of infection and number of cases of leishmaniasis. Parasitology Today 8, 104105.CrossRefGoogle ScholarPubMed
Behura, S.K., Sahu, S.C., Mohan, M. & Nair, S. (2001) Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): correlation between host mitotypes and infection status. Insect Molecular Biology 10, 163171.CrossRefGoogle ScholarPubMed
Braig, H.K., Guzman, H., Tesh, R.B. & O'Neill, S.L. (1994) Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367, 453455.CrossRefGoogle ScholarPubMed
Braig, H.K., Zhou, W., Dobson, S.L. & O'Neill, S.L. (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology 180, 23732378.CrossRefGoogle ScholarPubMed
Cheng, Q., Ruel, T.D., Zhou, W., Moloo, S.K., Majiwa, P., O'Neill, S.L. & Aksoy, S. (2000) Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Medical and Veterinary Entomology 14, 4455.CrossRefGoogle ScholarPubMed
Cui, L., Chang, S.H., Stickman, D. & Rowton, E. (1999) Frequency of Wolbachia infection in laboratory and field sand fly (Diptera: Psychodidae) populations. Journal of the American Mosquito Control Association 15, 571572.Google ScholarPubMed
Curtis, C.F. & Sinkins, S.P. (1998) Wolbachia as a possible means of driving genes into populations. Parasitology 116, S111–115.CrossRefGoogle ScholarPubMed
Dobson, S.L., Bourtzis, K., Braig, H.R., Jones, B.F., Zhou, W., Rousset, F. & O'Neill, S.L. (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochemistry and Molecular Biology 29, 153160.CrossRefGoogle ScholarPubMed
Egyed, Z., Sréter, T., Széll, Z., Nyirö, G., Márialigeti, K. & Varga, I. (2002) Molecular phylogenetic analysis of Onchocerca lupi and its Wolbachia endosymbiont. Veterinary Parasitology 108, 153161.CrossRefGoogle ScholarPubMed
Esseghir, S., Ready, P.D., Killick-Kendrick, R. & Ben-Ismail, R. (1997) Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Molecular Biology 6, 211225.CrossRefGoogle ScholarPubMed
Esseghir, S., Ready, P.D. & Ben-Ismail, R. (2000) Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biological Journal of the Linnean Society 70, 189219.CrossRefGoogle Scholar
Guillemaud, T., Pasteur, N. & Rousset, F. (1997) Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens. Proceedings of the Royal Society of London series B 264, 245251.CrossRefGoogle ScholarPubMed
Hoffmann, A.A. & Turelli, M. (1988) Unidirectional incompatibility in Drosophila simulans: inheritance, geographic variation and fitness effects. Genetics 119, 435444.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Clancy, D. & Duncan, J. (1996) Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76, 18.CrossRefGoogle Scholar
Jeyaprakash, A. & Hoy, M.A. (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology 9, 393405.CrossRefGoogle ScholarPubMed
Kittayapong, P., Baisley, K.J., Baimai, V. & O'Neill, S. (2000) Distribution and diversity of Wolbachia infections in southeast Asian mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 37, 340345.CrossRefGoogle ScholarPubMed
Lewis, D.J. (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodidae). Bulletin of the British Museum (Natural History) (Entomology) 45, 121209.Google Scholar
Mahamdallie, S.S., Pesson, B., Morillas-Marquez, F., Perrotey, S. & Ready, P.D. (2003) Adaptive variation in fringe populations of Phlebotomus perniciosus, an important vector of leishmaniasis in Europe. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, in press.Google Scholar
Marcadé, I., Souty-Grosset, C., Bouchon, D., Rigaud, T. & Raimond, R. (1999) Mitochondrial DNA variability and Wolbachia infection in two sibling woodlice species. Heredity 83, 7178.CrossRefGoogle Scholar
Mitsuhashi, W., Saiki, T., Wei, W., Kawakita, H. & Sato, M. (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Molecular Biology 11, 577584.CrossRefGoogle ScholarPubMed
Noda, H., Koizumi, Y., Zhang, Q. & Deng, K. (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochemistry and Molecular Biology 31, 727737.CrossRefGoogle ScholarPubMed
O'Neill, S.L., Giordano, R., Colbert, A.M., Karr, T.L. & Robertson, H.M. (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplamic incompatibility in insects. Proceedings of the National Academy of Sciences of the USA 89, 26992702.CrossRefGoogle Scholar
O'Neill, S.L., Pettigrew, M.M., Sinkins, S.P., Braig, H.R., Andrealis, T.G. & Tesh, R.B. (1997) In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Molecular Biology 6, 3339.CrossRefGoogle Scholar
Ono, M., Braig, H.R., Munstermann, L.E., Ferro, C. & O'Neill, S.L. (2001) Wolbachia infections of phlebotomine sand flies (Diptera: Psychodidae). Journal of Medical Entomology 38, 237241.CrossRefGoogle ScholarPubMed
Parvizi, P., Benlarbi, M. & Ready, P.D. (2003) Maternally-inherited DNA markers (cytochrome b and wsp) for Phlebotomus papatasi from domestic sites and gerbil burrows in Isfahan province, Iran. Transactions of the Royal Society of Tropical Medicine & Hygiene 97, in press.Google Scholar
Ready, P.D., Lainson, R., Shaw, J.J. & Souza, A.A. (1991) DNA probes for distinguishing Psychodopygus wellcomei from Psychodopygus complexus (Diptera: Psychodidae). Memórias do Instituto Oswaldo Cruz 86, 4149.CrossRefGoogle ScholarPubMed
Saraiva, E., Fampa, P., Cedeno, V., Bergoin, M., Mialhe, E. & Miller, L.H. (2000) Expression of heterologous promoters in Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae) cell lines. Journal of Medical Entomology 37, 802806.CrossRefGoogle ScholarPubMed
Shoemaker, D.D., Ross, K.G., Keller, L., Vargo, E.L. & Werren, J.H. (2000) Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). Insect Molecular Biology 9, 661673.CrossRefGoogle ScholarPubMed
Sinkins, S.P., Braig, H.R. & O'Neill, S.L. (1995 a) Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Experimental Parasitology 81, 284291.CrossRefGoogle ScholarPubMed
Sinkins, S.P., Braig, H.R. & O'Neill, S.L. (1995 b) Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proceedings of the Royal Society of London series B 261, 325330.Google ScholarPubMed
Sironi, M., Bandi, C., Sacchi, L., Di Sacco, B., Damiani, G. & Genchi, C. (1995) Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Molecular and Biochemical Parasitology 74, 223227.CrossRefGoogle Scholar
Testa, J.M., Montoya-Lerma, J., Cadena, H., Oviedo, M. & Ready, P.D. (2002) Molecular identification of vectors of Leishmania in Colombia: mitochondrial introgression in the Lutzomyia townsendi series. Acta Tropica 84, 205218.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440442.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140, 13191338.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1999) Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Molecular Biology 8, 243255.Google ScholarPubMed
Turelli, M., Hoffmann, A.A. & McKechnie, S.W. (1992) Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132, 713723.CrossRefGoogle ScholarPubMed
Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. & Bouletreau, M. (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Molecular Biology and Evolution 16, 17111723.CrossRefGoogle ScholarPubMed
Wade, M.J. (2001) Infectious speciation. Nature 409, 675676.CrossRefGoogle ScholarPubMed
Weeks, A.R., Reynolds, K.T. & Hoffmann, A.A. (2002) Wolbachia dynamics: what has (and has not) been demonstrated? TRENDS in Ecology and Evolution 17, 257262.CrossRefGoogle Scholar
Zhou, W., Rousset, F. & O'Neill, S. (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London series B 265, 509515.CrossRefGoogle ScholarPubMed