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Parasitology Research

, Volume 110, Issue 5, pp 1765–1771 | Cite as

Molecular differentiation of Culicoides biting midges (Diptera: Ceratopogonidae) from the subgenus Culicoides Latreille in Denmark

  • S. B. Lassen
  • S. Achim Nielsen
  • H. Skovgård
  • M. Kristensen
Original Paper

Abstract

Identification of Culicoides biting midges to species has attracted attention due to the recent outbreak of bluetongue disease in Northern Europe. Identification of Culicoides to species level has been based on morphological characters and is difficult as several species belonging to species complexes are hard to distinguish. We evaluated the use of the mitochondrial DNA cytochrome oxidase I gene (COI) barcode region in the identification of species within the subgenus Culicoides. COI barcode sequence divergence within species was <1%, whereas it ranged from 12.5% to 19.8% between subgenus Culicoides species. The divergence of subgenus Culicoides species to C. nubeculosus from the subgenus Monoculicoides ranged from 24.4% to 26.1%. Specimens were differentiated into eight unique clusters, including the four common Palaearctic species Culicoides punctatus, Culicoides pulicaris, Culicoides impunctatus, and Culicoides grisescens. Additionally, this study confirms the existence of Culicoides halophilus as a valid taxon and presents the first Culicoides deltus barcode sequences. Three additional groups of specimens were identified: Culicoides dk1 with a COI barcode diverging by 14.3% to 17.2% from other subgenus Culicoides species and Culicoides Kalix and Culicoides dk3, which diverged by 5.9% from each other and showed 12.5% to 17.6% divergence in COI barcode to subgenus Culicoides specimens.

Keywords

British Isle Culicoides Species Valid Taxon Gamma Distribution Shape Parameter Midge Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The project was supported by the Danish Ministry of Food, Agriculture and Fisheries: 3304-FVFP-07-772-01. We thank Mette Knorr for the difficult task of coordinating placement of traps. We thank Claus Dahl and Högni Holm for their untiring efforts in collection and sorting of biting midges. We also thank an anonymous reviewer for useful comments on an earlier version of the manuscript.

References

  1. Bitanyi S, Bjørnstad G, Ernest EM, Nesje M, Kusiluka LJ, Keyyu JD, Mdegela RH, Røed KH (2011) Species identification of Tanzanian antelopes using DNA barcoding. Mol Ecol Res 11:442–449CrossRefGoogle Scholar
  2. Borkent A (2011) World species of biting midges (Diptera: Ceratopogonidae). Available at http://www.inhs.illinois.edu/research/FLYTREE/CeratopogonidaeCatalog.pdf. Accessed 10 Feb 2011
  3. Campbell JA, Pelham-Clinton EC (1960) A taxonomic review of the British species of Culicoides Latreille (Diptera, Ceratopogonidae). Proc Roy Soc Edinb B67:181–302Google Scholar
  4. Casati S, Racloz V, Delècolle JC, Kuhn M, Mathis A, Griot C, Stärk KDC, Vanzetti T (2009) An investigation on the Culicoides species composition at seven sites in southern Switzerland. Med Vet Entomol 23:93–98PubMedCrossRefGoogle Scholar
  5. Dzhafarov SH (1976) Biting midges (Diptera, Heleidae) of transcaucasus (morphology, biology, ecology, geographical distribution, and harmfulness, control, fauna of the genera Culicoides, Leptoconops and Lasiohelea). Publishing House of the Academy of Science of Azerbaijan SSR.Translated for the Agricultural Research Service, U.S. Department of Agriculture, and the National Science Foundation Washington, D.C. by Franklin Book Programs. Inc., Cairo, 1976Google Scholar
  6. Glukhova VM (2005) Culicoides (Diptera: Ceratopogonidae) of Russia and adjacent lands. Int J Dipterol Res 16:3–75Google Scholar
  7. Gomulski LM, Meiswinkel R, Delélecolle JC, Goffredo M, Gasperi G (2005) Phylogenetic relationships of the genus Avaritia Fox, 1955 including Culicoides obsoletus (Diptera, Ceratopogonidae) in Italy based on internal spacer 2 ribosomal DNA sequences. Syst Entomol 30:619–631CrossRefGoogle Scholar
  8. Gomulski LM, Meiswinkel R, Delélecolle JC, Goffredo M, Gasperi G (2006) Phylogeny of the subgenus Culicoides and related species in Italy, inferred from internal transcribed spacer 2 ribosomal DNA sequences. Med Vet Entomol 20:229–238PubMedCrossRefGoogle Scholar
  9. Handfield D, Handfield L (2006) A new species of Plusia (Lepidoptera: Noctuidae) from North America. Can Entomol 138:853–859CrossRefGoogle Scholar
  10. Hebert PDN, deWaard JR, Landry JF (2010) DNA barcodes from 1/1000 of the animal kingdom. Biol Lett 6:359–362PubMedCrossRefGoogle Scholar
  11. Kiel E, Liebisch G, Focke R, Liebisch A, Werner D (2009) Monitoring Culicoides at 20 localities in northwest Germany. Parasitol Res 105(351–357):591CrossRefGoogle Scholar
  12. Kremer M (1965) Contribution à l`étude du genre Culicoides Latreille particulièrement en France. Encycl Ent A 39:1–299Google Scholar
  13. Lakra WS, Goswami M, Gopalakrishnan A (2009) Molecular identification and phylogentic relationship of seven Indian Sciaenids (Pisces: Perciformes, Sciaenidae) based on 16S rRNA and cytochrome c oxidase subunit I mitochondrial genes. Mol Biol Rep 36:831–836PubMedCrossRefGoogle Scholar
  14. Lassen SB, Nielsen SA, Skovgård H, Kristensen M (2011) Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitol Res 108:823–829PubMedCrossRefGoogle Scholar
  15. Mathieu B, Perrin A, Baldet T, Delélecolle JC, Albina E, Cêtre-Sossah C (2007) Molecular identification of Western European species of Obsoletus complex (Diptera: Ceratopogonidae) by an internal transcribed spacer-1 rDNA multiplex polymerase chain reaction assay. J Med Entomol 44:1019–1025PubMedCrossRefGoogle Scholar
  16. Meiswinkel R, Gomulski LM, Delécolle JC, Goffredo M, Gasperi G (2004) The taxonomy of Culicoides vector complexes—unfinished business. Vet Ital 40:151–159PubMedGoogle Scholar
  17. Meiswinkel R, Goffredo M, Leijs P, Conte A (2008) The Culicoides ‘snapshot’: a novel approach used to assess vector densities widely and rapidly during the 2006 outbreak of bluetongue (BT) in The Netherlands. Prev Vet Med 87:98–118PubMedCrossRefGoogle Scholar
  18. Mellor PS, Boorman J, Baylis M (2000) Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol 45:307–340PubMedCrossRefGoogle Scholar
  19. Muñoz-Muñoz F, Talavera S, Pagès N (2011) Geometric morphometrics of the wing in the subgenus Culicoides (Diptera: Ceratoponidae): from practical implications to evolutionary interpretations. J Med Entomol 48:129–139PubMedCrossRefGoogle Scholar
  20. Nielsen SA, Kristensen M (2011) Morphological and molecular identification of species of the Obsoletus group (Diptera: Ceratopogonidae) in Scandinavia. Parasitol Res 109:1133–1141PubMedCrossRefGoogle Scholar
  21. Nielsen SA, Nielsen BO, Chirico J (2010) Monitoring of biting midges (Diptera: Culicoides Latreille) on farms in Sweden during the emergence of the 2008 epidemic of bluetongue. Parasitol Res 106:1197–1203PubMedCrossRefGoogle Scholar
  22. Nolan DV, Carpenter S, Barber J, Mellor PS, Dallas JF, Mordue Luntz AJ, Piertney SB (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Vet Microbiol 124:82–94PubMedCrossRefGoogle Scholar
  23. Pagès N, Sarto i Monteys V (2005) Differentiation of Culicoides obsoletus and Culicoides scoticus (Diptera: Ceratopogonidae) based on mitochondrial cytochrome oxidase subunit I. J Med Entomol 42:1026–1034PubMedCrossRefGoogle Scholar
  24. Pagès N, Muñoz-Muñoz F, Talavera S, Sarto V, Lorca C, Núñez JI (2009) Identification of cryptic species of Culicoides (Diptera: Ceratopogonidae) in the subgenus Culicoides and development of species-specific PCR assays based on barcode regions. Vet Parasitol 165:298–310PubMedCrossRefGoogle Scholar
  25. Remm H (1988) Ceratopogonidae. In: Soos A, Papp L (eds) Catalogue of Palaearctic Diptera, vol 3. Akadémiai Kiadó, Budapest, pp 11–110Google Scholar
  26. Takken W, Verhulst N, Scholte EJ, Jacobs F, Jongema Y, van Lammeren R (2008) The phenology and population dynamics of Culicoides spp. in different ecosystems in The Netherlands. Prev Vet Med 87:41–54PubMedCrossRefGoogle Scholar
  27. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  28. Vorsprach B, Meiser CK, Werner D, Balczun C, Schaub GA (2009) Monitoring of Ceratopogonidae in Southwest Germany. Parasitol Res 105:337–344PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • S. B. Lassen
    • 1
  • S. Achim Nielsen
    • 2
  • H. Skovgård
    • 1
  • M. Kristensen
    • 1
  1. 1.Department of AgroecologyAarhus UniversitySlagelseDenmark
  2. 2.Department of Environmental, Social and Spatial ChangeRoskilde UniversityRoskildeDenmark

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