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Variations in the mitochondrial cytochrome c oxidase subunit I gene indicate northward expanding populations of Culicoides imicola in Spain

Published online by Cambridge University Press:  19 February 2009

J.H. Calvo ,
C. Calvete ,
A. Martinez-Royo ,
R. Estrada ,
M.A. Miranda ,
D. Borras ,
V. Sarto I Monteys ,
N. Pages ,
J.A. Delgado  and
F. Collantes
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J.H. Calvo*
Affiliation:
Unidad de Tecnología en Producción animal, CITA-ARAID, Zaragoza, Spain
C. Calvete
Affiliation:
Unidad Sanidad Animal, CITA, Zaragoza. Spain
A. Martinez-Royo
Affiliation:
Unidad de Tecnología en Producción animal, CITA-ARAID, Zaragoza, Spain
R. Estrada
Affiliation:
Departamento de Patología Animal, Universidad de Zaragoza, Zaragoza, Spain
M.A. Miranda
Affiliation:
Laboratorio de Zoología, Universidad de las Islas Baleares, Palma de Mallorca, Spain
D. Borras
Affiliation:
Laboratorio de Zoología, Universidad de las Islas Baleares, Palma de Mallorca, Spain
V. Sarto I Monteys
Affiliation:
Unidad de Entomología. Fundación CReSA, UAB Bellaterra, Spain
N. Pages
Affiliation:
Unidad de Entomología. Fundación CReSA, UAB Bellaterra, Spain
J.A. Delgado
Affiliation:
Departamento de Zoología y Antropología Física, Universidad de Murcia, Murcia, Spain
F. Collantes
Affiliation:
Departamento de Zoología y Antropología Física, Universidad de Murcia, Murcia, Spain
J. Lucientes
Affiliation:
Departamento de Patología Animal, Universidad de Zaragoza, Zaragoza, Spain
*
*Author for correspondence Fax: +34 976716335 E-mail: jhcalvo@aragon.es
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Abstract

Culicoides imicola is the main vector for bluetongue (BT) and African horse sickness (AHS) viruses in the Mediterranean basin and in southern Europe. In this study, we analysed partial mitochondrial cytochrome c oxidase subunit I (COI) gene to characterize and confirm population expansion of Culicoides imicola across Spain. The data were analysed at two hierarchical levels to test the relationship between C. imicola haplotypes in Spain (n=215 from 58 different locations) and worldwide (n=277). We found nineteen different haplotypes within the Spanish population, including 11 new haplotypes. No matrilineal subdivision was found within the Spanish population, while western and eastern Mediterranean C. imicola populations were very structured. These findings were further supported by median networks and mismatch haplotype distributions. Median networks demonstrated that the haplotypes we observed in the western Mediterranean region were closely related with one another, creating a clear star-like phylogeny separated only by a single mutation from eastern haplotypes. The two, genetically distinct, sources of C. imicola in the Mediterranean basin, thus, were confirmed. This type of star-like population structure centred around the most frequent haplotype is best explained by rapid expansion. Furthermore, the proposed northern expansion was also supported by the statistically negative Tajima's D and Fu's Fs values, as well as predicted mismatch distributions of sudden and spatially expanding populations. Our results thus indicated that C. imicola population expansion was a rapid and recent phenomenon.

Keywords

Culicoides imicolaAfrican horse sicknessbluetonguecytochrome c oxidase Ipopulation expansionmtDNA
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 6 , December 2009 , pp. 583 - 591
Copyright
Copyright © 2009 Cambridge University Press

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References

Aris-Brosou, S. & Excoffier, L. (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology Evolution 13, 494–504.CrossRefGoogle ScholarPubMed
Braverman, J.M., Hudson, R.R., Kaplan, N.L., Langley, C.H. & Stephan, W. (1995) The hitchhiking effect on the site frequency-spectrum of DNA polymorphisms. Genetics 140 (2), 783–796.CrossRefGoogle ScholarPubMed
Calistri, P., Goffredo, M., Caporale, V. & Meiswinkel, R. (2003) The distribution of Culicoides imicola in Italy: application and evaluation of current Meditteranean models based on climate. Journal of Veterinary Medicine B 50, 132–138.CrossRefGoogle Scholar
Calvete, C., Miranda, M.A., Estrada, R., Borras, D., Sarto, I., Monteys, V., Collantes, F., Garcia-de-Francisco, J.M., Moreno, N. & Lucientes, J. (2006) Spatial distribution of Culicoides imicola, the main vector of bluetongue virus, in Spain. Veterinary Record 158(4), 130–131.CrossRefGoogle ScholarPubMed
Calvete, C., Calvo, J.H., Calavia, R., Miranda, M.A., Borrás, D., Estrada, R., Lucientes, J., Mañuz, B. & Romero, L. (2008) Culicoides species and transmission of bluetongue virus in Spain. Veterinary Record 162, 255.CrossRefGoogle ScholarPubMed
Capela, R., Purse, B.V., Pena, I., Wittmann, F.J., Margarita, Y., Capela, M., Romao, L., Mellor, P.S. & Baylis, M. (2003) Spatial distribution of Culicoides species in Portugal in relation to the transmisión of African horse sickness and bluetongue viruses. Medical and Veterinary Entomology 17, 165–177.CrossRefGoogle Scholar
Dallas, J.F., Cruickshank, R.H., Linton, Y.M., Nolan, D.V., Patakakis, M., Braverman, Y., Capela, R., Capela, M., Pena, I., Meiswinkel, R., Ortega, M.D., Baylis, M., Mellor, P.S. & Mordue, A.J. (2003) Phylogenetic status and matrilineal structure of the biting midge, Culicoides imicola, in Portugal, Rhodes and Israel. Medical and Veterinary Entomology 17, 379–387.CrossRefGoogle ScholarPubMed
De Liberato, C., Scavia, G., Lorenzetti, R., Scaramozzino, P., Amaddeo, D., Cardeti, G., Scicluna, M., Ferrari, G. & Autorino, G.L. (2005) Identification of Culicoides obsoletus (Diptera: Ceratopogonidae) as a vector of bluetongue virus in central Italy. The Veterinary Record 156, 301–304.CrossRefGoogle ScholarPubMed
Du Toit, R.M. (1944) The transmission of blue-tongue and horsesickness by Culicoides. Onderstepoort Journal of Veterinary Science and Animal Industry 19, 7–16.Google Scholar
Excoffier, L. (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology 13(4), 853–864.CrossRefGoogle ScholarPubMed
Gomez-Tejedor, C. (2004) Brief overview of the bluetongue situation in Mediterranean Europe, 1998–2004. Veterinaria Italiana 40(3), 57–60.Google ScholarPubMed
Gomulski, L.M., Meiswinkel, R., Delecolle, J.C., Goffredo, M. & Gasperi, G. (2005) Phylogenetic relationships of the subgenus Avaritia Fox, 1955 including Culicoides obsoletus (Diptera, Ceratopogonidae) in Italy based on internal transcribed spacer 2 ribosomal DNA sequences. Systematic Entomology 30(4), 619–631.CrossRefGoogle Scholar
Gomulski, L.M., Meiswinkel, R., Delecolle, J.C., Goffredo, M. & Gasperi, G. (2006) Phylogeny of the subgenus Culicoides and related species in Italy, inferred from internal transcribed spacer 2 ribosomal DNA sequences. Medical and Veterinary Entomology 20(2), 229–238.CrossRefGoogle ScholarPubMed
Hahn, M.W., Rausher, M.D. & Cunningham, C.W. (2002) Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161(1), 11–20.CrossRefGoogle Scholar
Harpending, R.C. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591–600.Google Scholar
Holmes, I.H., Boccardo, G., Estes, M.K. & Furuichi, M.K. (1995). Family Reoviridae. pp. 208–239in Murphy, F.A., Fauquet, C.M., Bishop, D.H.L. & Ghabrial, S.A. (Eds) Virus taxonomy, classification and nomeclature of viruses. Sixth report of the international committee on taxonomy of viruses. Archives of Virology, Suppl. 10, Wien, New York, Springer.Google Scholar
Jennings, D.M., Boorman, J.P.T. & Ergün, H. (1983) Culicoides from Western Turkey in relation to bluetongue disease of sheep and cattle. Revue d'Elevage et de Mèdecine Vètérinaire des Pays Tropicaux 36, 67–70.Google ScholarPubMed
Kumar, S., Tamura, K., Jakobsen, I.B. & Nei, M. (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17(12), 1244–1245.CrossRefGoogle ScholarPubMed
Linton, Y.M., Mordue, A.J., Cruickshank, R.H., Meiswinkel, R., Mellor, P.S. & Dallas, J.F. (2002) Phylogenetic analysis of the mitochondrial cytochrome oxidase subunit I gene of five species of the Culicoides imicola species complex. Medical and Veterinary Entomology 16(2), 139–146.CrossRefGoogle Scholar
Manso-Ribeiro, J.J., Rosa-Azevedo, A., Noroña, F.O., Blanco-Forte, M.C., Grave-Pereira, C. & Vasco-Fernandez, M. (1957) Fiebre catarrhale du mouton (Bluetongue). Bulletin de l'Office International des Épizooties 48, 350–367.Google Scholar
Mehlhorn, H., Walldorf, V., Klimpel, S., Jahn, B., Jaeger, F., Eschweiler, J., Hoffmann, B. & Beer, M. (2007) First occurrence of Culicoides obsoletus-transmitted bluetongue virus epidemic in Central Europe. Parasitology Research 101, 219–228.CrossRefGoogle ScholarPubMed
Meiswinkel, R., van Rijn, P., Leijs, P. & Goffredo, M. (2007) Potential new Culicoides vector of bluetongue virus in northern Europe. Veterinary Record 161, 564–565.CrossRefGoogle ScholarPubMed
Meiswinkel, R., Baldet, T., de Deken, R., Takken, W., Delecolle, J.C. & Mellor, P.S. (2008) The 2006 outbreak of bluetongue in northern Europe: The entomological perspective. Preventive Veterinary Medicine 87(1–2), 55–63.CrossRefGoogle ScholarPubMed
Mellor, P.S. (1996) Culicoides: vectors, climate change and disease risk. Veterinary Bulletin 66, 301–306.Google Scholar
Mellor, P.S. & Pitzolis, G. (1979) Observations on breeding sites and light trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bulletin of Entomological Research 69, 229–234.CrossRefGoogle Scholar
Mellor, P.S. & Wittmann, E.J. (2002) Bluetongue virus in the Mediterranean basin 1998–2001. Veterinary Journal 164, 20–37.CrossRefGoogle ScholarPubMed
Mellor, P.S., Boned, J., Hamblin, C. & Graham, S. (1990) Isolations of African horse sickness virus from vector insects made during the 1988 epizootic in Spain. Epidemiology and Infection 105, 447–454.CrossRefGoogle ScholarPubMed
Miranda, M.A., Borras, D., Rincon, C. & Alemany, A. (2003) Presence in the Balearic Islands (Spain) of the midges Culicoides imicola and Culicoides obsoletus group. Medical and Veterinary Entomology 17, 52–54.CrossRefGoogle ScholarPubMed
Nei, M. & Li, W.H. (1979) Mathematical model for studying genetic-variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America 76(10), 5269–5273.CrossRefGoogle ScholarPubMed
Nolan, D.V., Carpenter, S., Barber, J., Mellor, P.S., Dallas, J.F., Mordue, A.J., Mordue, A.J. & Piertney, S.B. (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Veterinary Microbiology 124(1–2), 82–94.CrossRefGoogle ScholarPubMed
Office International des Epizooties (OIE) (2000) Bluetongue in Spain: in the Balearic Islands. Follow-up report No. 1. Disease Information 13, 224.Google Scholar
Ortega, M.D., Holbrook, F.R. & Lloyd, J.E. (1999) Seasonal distribution and relationship to temperature and precipitation of the most abundant species of Culicoides in five provinces of Andalusia, Spain. Journal of the American Mosquito Control Association 15(3), 391–399.Google ScholarPubMed
Perrin, A., Cetre-Sossah, C., Mathieu, B., Baldet, T., Delecolle, J.C. & Albina, E. (2006) Phylogenetic analysis of Culicoides species from France based on nuclear ITS1-rDNA sequences. Medical and Veterinary Entomology 20(2), 219–228.CrossRefGoogle ScholarPubMed
Rawlings, P. (1996) A key, based on wing patterns of biting midges (genus Culicoides Latreille – Diptera: Ceratopogonidae) in the Iberian Peninsula, for use in epidemiological studies. Graellsia 52, 57–71.CrossRefGoogle Scholar
Rawlings, P., Pro, M.J., Peña, L., Ortega, M.D. & Capela, R. (1997) Spatial and seasonal distribution of Culicoides imicola in Iberia in relation to the transmission of African horse sickness virus. Medical and Veterinary Entomology 11, 49–57.CrossRefGoogle Scholar
Ray, N., Currat, M. & Excoffier, L. (2003) Intra-Deme Molecular Diversity in Spatially Expanding Populations. Molecular Biology and Evolution 20(1), 76–86.CrossRefGoogle ScholarPubMed
Rich, S.M., Licht, M.C., Hudson, R.R. & Ayala, F.J. (1998) Malaria's Eve: Evidence of a recent population bottleneck throughout the world population of Plasmodium falciparum. Proceedings of the National Academy of Sciences of the United States of America 95, 4425–4430.CrossRefGoogle ScholarPubMed
Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.Google ScholarPubMed
Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19(18), 2496–2497.CrossRefGoogle ScholarPubMed
Sarto I Monteys, V., Ventura, D., Pages, N., Aranda, C. & Escosa, R. (2005) Expansion of Culicoides imicola, the main bluetongue virus vector in Europe, into Catalonia, Spain. Veterinary Record 156, 415–417.CrossRefGoogle ScholarPubMed
Schneider, S. & Excoffier, L. (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetics 152, 1079–1089.CrossRefGoogle ScholarPubMed
Slatkin, M. & Hudson, R.R. (1991) Pairwise comparisons of mitochondrial-DNA sequences is stable and sponentially growing populations. Genetics 129(2), 555–562.CrossRefGoogle ScholarPubMed
Tabachnick, W.J. & Black, W.C. (1995) Making a case for molecular population genetic-studies of arthropod vectors. Parasitology Today 11(1), 27–30.CrossRefGoogle Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Takamatsu, H., Mellor, P.S., Mertens, P.P.C., Kirkham, P.A., Burroughs, J.N. & Parkhouse, R.M.E. (2003) A possible overwintering mechanism for bluetongue virus in the absence of the insect vector. Journal of general Virology 84, 227–235.CrossRefGoogle ScholarPubMed
Walker, D.E., Moler, P.E., Buhlmann, K.A. & Avise, J.C. (1998) Phylogeographic uniformity in mitochondrial DNA of the snapping turtle (Chelydra serpentina). Animal Conservation 1, 55–60.CrossRefGoogle Scholar
Watterson, G.A. (1975) Number of segregating sites in genetic models without recombination. Theorical Population Biology 7(2), 256–276.CrossRefGoogle ScholarPubMed
Wittmann, E.J., Mellor, P.S. & Baylis, M. (2001) Using climate data to map the potential distribution of Culicoides imicola (Diptera: Ceratopogonidae) in Europe. Revue Scientifique et Technique de l'Office International des Epizooties 20, 731–740.CrossRefGoogle ScholarPubMed