Parasitology Research

, Volume 113, Issue 9, pp 3201–3210 | Cite as

Distribution and genetic structure of Aedes japonicus japonicus populations (Diptera: Culicidae) in Germany

  • Katrin Huber
  • Kathrin Schuldt
  • Martin Rudolf
  • Marco Marklewitz
  • Dina M. Fonseca
  • Christian Kaufmann
  • Yoshio Tsuda
  • Sandra Junglen
  • Andreas Krüger
  • Norbert Becker
  • Egbert Tannich
  • Stefanie C. BeckerEmail author
Original Paper


In recent years, the number of imported cases of arthropod-borne diseases in Europe, such as dengue fever, has increased steadily, as did the emergence and distribution of invasive insect vectors. Consequently, the risk of disease spreading into previously unaffected regions through invasive mosquitoes is also increasing. One example of an invasive mosquito is Aedes japonicus japonicus (A. j. japonicus), which spread from its original habitat in Japan to North America and Europe. This species has been shown to act as a vector for Japanese encephalitis and West Nile viruses. In Europe, A. j. japonicus has been detected in Switzerland, Belgium, Slovenia, and Germany, where it has become a resident species. Here, we describe the recent spread and genetic structure of A. j. japonicus populations in Germany. By monitoring the species in Baden-Württemberg in 2011 and 2012, we observed a considerable enlargement of the infested area from 54 municipalities in 2011 to 124 municipalities in 2012. To elucidate the colonization of Europe by A. j. japonicus, seven microsatellite loci were studied in 106 individuals sampled in Germany and Switzerland in 2012. The same markers were genotyped in 31 North American and 26 Japanese specimens. Population genetic analyses indicated that A. j. japonicus in Baden-Württemberg and North Rhine-Westphalia represented two genetically distinct populations with FST—values of 0.073–0.152, suggesting that they originated from two independent introduction events in the past. These results are of particular interest in light of vectorial variability for the transmission of viruses and other pathogens in Europe.


Aedes japonicus japonicus Pathogen Population 



We are grateful to Dr. Jonas Schmidt-Chanasit and Stephanie Jansen for the productive discussions and critical reading of the manuscript. This work was financially supported by the Leibniz Association, grant number SAW-2011-BNI-3, and the German Federal Ministry for Environment, Nature Conservation, Building and Nuclear Safety (BMUB) through the Federal Environment Agency (UBA), grant number FKZ371148404.

Supplementary material

436_2014_4000_MOESM1_ESM.doc (78 kb)
Table S1 (DOC 77 kb)


  1. Angelini R, Finarelli AC, Angelini P, Po C, Petropulacos K, Macini P, Fiorentini C, Fortuna C, Venturi G, Romi R, Majori G, Nicoletti L, Rezza G, Cassone A (2007) An outbreak of chikungunya fever in the province of Ravenna, Italy. Eur Surveill 12, E070906.1Google Scholar
  2. Becker N, Pluskota B, Kaiser A (2011) Ochlerotatus japonicus japonicus—a newly established neozoan in Germany and a revised list of the German mosquito fauna. Eur Mosq Bull 29:88–102Google Scholar
  3. Becker N, Geier M, Balczun C, Bradersen U, Huber K, Kiel E, Krüger A, Lühken R, Orendt C, Plenge-Bönig A, Rose A, Schaub GA, Tannich E (2013) Repeated introduction of Aedes albopictus into Germany, July to October 2012. Parasitol Res 112:1787–1790PubMedCrossRefGoogle Scholar
  4. Carrieri M, Bellini R, Maccaferri S, Gallo L, Maini S, Celli G (2008) Tolerance thresholds for Aedes albopictus and Aedes caspius in Italian urban areas. J Am Mosq Control Assoc 24:377–386PubMedCrossRefGoogle Scholar
  5. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  6. Felsenstein J (1989) PHYLIP—Phylogeny Inference Package. Cladistics 5:164–166Google Scholar
  7. Fonseca DM, Campbell S, Crans WJ, Mogi M, Miyagi I, Toma T, Bullians M, Andreadis TG, Berry RL, Pagac B, Sardelis MR, Wilkerson RC (2001) Aedes (Finlaya) japonicus (Diptera: Culicidae), a newly recognized mosquito in the United States: analyses of genetic variation in the United States and putative source populations. J Med Entomol 38:135–146PubMedCrossRefGoogle Scholar
  8. Fonseca DM, Widdel AK, Hutchinson M, Spichiger SE, Kramer LD (2010) Fine-scale spatial and temporal population genetics of Aedes japonicus, a new US mosquito, reveal multiple introductions. Mol Ecol 19:1559–1572PubMedCrossRefGoogle Scholar
  9. Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS One 7:e45170PubMedCentralPubMedCrossRefGoogle Scholar
  10. Hubalek Z (2008) Mosquito-borne viruses in Europe. Parasitol Res 103(Suppl 1):S29–S43PubMedCrossRefGoogle Scholar
  11. Huber K, Pluskota B, Jöst A, Hoffmann K, Becker N (2012) Status of the invasive species Aedes japonicus japonicus (Diptera: Culicidae) in southwest Germany in 2011. J Vector Ecol 37:462–465PubMedCrossRefGoogle Scholar
  12. Kampen H, Zielke D, Werner D (2012) A new focus of Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) distribution in Western Germany: rapid spread or a further introduction event? Parasitol Vectors 5:284CrossRefGoogle Scholar
  13. Karesh WB, Cook RA, Bennett EL, Newcomb J (2005) Wildlife trade and global disease emergence. Emerg Infect Dis 11:1000–1002PubMedCentralPubMedCrossRefGoogle Scholar
  14. Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53:61–81PubMedCrossRefGoogle Scholar
  15. Krida G, Bouattour A, Rodhain F, Failloux AB (1998) Variability among Tunisian populations of Culex pipiens: genetic structure and susceptibility to a filarial parasite, Brugia pahangi. Parasitol Res 84:139–142PubMedCrossRefGoogle Scholar
  16. Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H, Van Bortel W (2012) A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Dis 12:435–447PubMedCentralPubMedCrossRefGoogle Scholar
  17. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentralPubMedCrossRefGoogle Scholar
  18. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  19. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  20. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci U S A 94:9197–9201PubMedCentralPubMedCrossRefGoogle Scholar
  21. Raymond M, Rousset F (1995) Population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  22. Reinert JF (2000) New classification for the composite genus Aedes (Diptera: Culicidae: Aedini), elevation of subgenus Ochlerotatus to generic rank, reclassification of the other subgenera, and notes on certain subgenera and species. J Am Mosq Control Assoc 16:175–188PubMedGoogle Scholar
  23. Schaffner F, Chouin S, Guilloteau J (2003) First record of Ochlerotatus (Finlaya) japonicus japonicus (Theobald, 1901) in metropolitan France. J Am Mosq Control Assoc 19:1–5PubMedGoogle Scholar
  24. Schaffner F, Kaufmann C, Hegglin D, Mathis A (2009) The invasive mosquito Aedes japonicus in Central Europe. Med Vet Entomol 23:448–451PubMedCrossRefGoogle Scholar
  25. Schaffner F, Kaufmann C, Failloux AB, Mathis A (2011) Vector competence of Aedes japonicus for chikungunya and dengue viruses. Eur Mosq Bull 29:141–142Google Scholar
  26. Schmidt-Chanasit J, Tenner-Racz K, Poppert D, Emmerich P, Frank C, Dinges C, Penning R, Nerlich A, Racz P, Günther S (2012) Fatal dengue hemorrhagic fever imported into Germany. Infection 40:441–443PubMedCrossRefGoogle Scholar
  27. Schneider K (2011) Breeding of Ochlerotatus japonicus japonicus (Diptera: Culicidae) 80 km north of its known range in southern Germany. Eur Mosq Bull 29:129–132Google Scholar
  28. Seidel B, Duh D, Nowotny N, Allerberger F (2012) First record of the mosquitoes Aedes (Ochlerotatus) japonicus japonicus (Theobald, 1901) in Austria and Slovenia 2011 and for Aedes (Stegomyia) albopictus (Skuse, 1895) in Austria. Entomol Z Insektenborse 122:223–226Google Scholar
  29. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629PubMedCrossRefGoogle Scholar
  30. Takashima I, Rosen L (1989) Horizontal and vertical transmission of Japanese encephalitis virus by Aedes japonicus (Diptera: Culicidae). J Med Entomol 26:454–458PubMedGoogle Scholar
  31. Tanaka K, Mizusawa K, Saugstad ES (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu archipelago and the Ogasawara islands) and Korea (Diptera: Culicidae). Contrib Am Entomol Inst 16:1–987Google Scholar
  32. Turell MJ, O'Guinn ML, Dohm DJ, Jones JW (2001) Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38:130–134PubMedCrossRefGoogle Scholar
  33. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  34. Versteirt V, Schaffner F, Garros C, Dekoninck W, Coosemans M, Van Bortel W (2009) Introduction and establishment of the exotic mosquito species Aedes japonicus japonicus (Diptera: Culicidae) in Belgium. J Med Entomol 46:1464–1467PubMedCrossRefGoogle Scholar
  35. Werner D, Kampen H (2013) The further spread of Aedes japonicus japonicus (Diptera, Culicidae) towards northern Germany. Parasitol Res 112:3665–3668PubMedCrossRefGoogle Scholar
  36. Werner D, Kronefeld M, Schaffner F, Kampen H (2012) Two invasive mosquito species, Aedes albopictus and Aedes japonicus japonicus, trapped in south-west Germany, July to August 2011. Euro Surveill 17Google Scholar
  37. Widdel AK, McCuiston LJ, Crans WJ, Kramer LD, Fonseca DM (2005) Finding needles in the haystack: single copy microsatellite loci for Aedes japonicus (Diptera: Culicidae). Am J Trop Med Hyg 73:744–748PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Katrin Huber
    • 1
    • 3
    • 4
  • Kathrin Schuldt
    • 2
  • Martin Rudolf
    • 1
  • Marco Marklewitz
    • 5
  • Dina M. Fonseca
    • 6
  • Christian Kaufmann
    • 7
  • Yoshio Tsuda
    • 8
  • Sandra Junglen
    • 5
  • Andreas Krüger
    • 9
  • Norbert Becker
    • 3
    • 4
  • Egbert Tannich
    • 1
    • 10
  • Stefanie C. Becker
    • 11
    Email author
  1. 1.Bernhard Nocht Institute for Tropical MedicineHamburgGermany
  2. 2.Department for Molecular MedicineBernhard Nocht Institute for Tropical MedicineHamburgGermany
  3. 3.German Mosquito Control Association (KABS/GFS)WaldseeGermany
  4. 4.University of HeidelbergHeidelbergGermany
  5. 5.University of Bonn Medical CentreBonnGermany
  6. 6.Rutgers UniversityNew BrunswickUSA
  7. 7.University of ZurichZurichSwitzerland
  8. 8.National Institute of Infectious DiseasesTokyoJapan
  9. 9.Bundeswehr Hospital HamburgHamburgGermany
  10. 10.Hamburg and German Centre for Infection Research, partner site Hamburg-Luebeck-BorstelHamburgGermany
  11. 11.Research Group EntomologyBernhard Nocht Institute for Tropical MedicineHamburgGermany

Personalised recommendations