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Clearing up Culex Confusion: A Basis for Virus Vector Discrimination in Europe
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Mosquito species of the Culex genus are the enzootic vectors for several bird-associated viruses that cause disease in humans. In Europe, these viruses include Sindbis (SINV), West Nile and Usutu viruses. The morphologically similar females of Cx. torrentium and Cx. pipiens are potential vectors of these viruses, but difficulties in correctly identifying the mosquito species have caused confusion regarding their respective distribution, abundance, ecology, and consequently their importance as vectors. Species-specific knowledge from correctly identified field material is however of crucial importance since previous research shows that the relatively unknown Cx. torrentium is a far more efficient SINV vector than the widely recognized Cx. pipiens. The latter is involved in the transmission of several other viruses, but its potential importance for SINV transmission is debated.

In this thesis I describe the development of a molecular method for species identification, based on reliably identified males of Cx. torrentium and Cx. pipiens. This identification method was then used in consecutive studies on the distribution and relative abundance of the two species in Sweden and 12 other European countries, SINV field infection rates in mosquitoes identified to species level, and evaluation of potential trap bias associated with common sampling techniques.

The results showed that Cx. torrentium is a far more common species in Europe than previously assumed. In Sweden and Finland, it is the dominant species, accounting for 89% of the sampled Culex population. In central Europe, it is equally common to Cx. pipiens, while Cx. pipiens dominates south of the Alps Mountain range. Larvae of both species are often found together in both artificial containers (e.g. car tires) and natural sites. Also, a trapping bias against Cx. torrentium was revealed for CDC-traps. For the first time, SINV was isolated from species-identified Cx. torrentium and Cx. pipiens mosquitoes caught in the field, with Cx. torrentium being superior in infection rates (36/1,000 vs. 8.2/1,000). Future studies on SINV, as well as other mosquito-borne bird viruses in Europe, can hopefully gain from the baseline information provided here, and from principles of vector discrimination discussed in the thesis.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. , 56 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1185
Keyword [en]
Culex torrentium, Culex pipiens, mosquitoes, vector, ornithophilic, Sindbis virus, West Nile virus
National Category
Biological Sciences
Research subject
Population Biology
Identifiers
URN: urn:nbn:se:uu:diva-232726ISBN: 978-91-554-9044-7 (print)OAI: oai:DiVA.org:uu-232726DiVA: diva2:749384
Public defence
2014-11-07, Zootissalen, Villavägen 9, 2 tr, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2014-10-17 Created: 2014-09-23 Last updated: 2015-01-23
List of papers
1. A sensitive and reliable restriction enzyme assay to distinguish between the mosquitoes Culex torrentium and Culex pipiens
Open this publication in new window or tab >>A sensitive and reliable restriction enzyme assay to distinguish between the mosquitoes Culex torrentium and Culex pipiens
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2010 (English)In: Medical and Veterinary Entomology, ISSN 0269-283X, E-ISSN 1365-2915, Vol. 24, no 2, 142-149 p.Article in journal (Refereed) Published
Abstract [en]

Culex pipiens pipiens Linnaeus and Culex torrentium Martini (Diptera: Culicidae) are closely related vector species that exist sympatrically in Europe. The two species are morphologically almost identical and can only be distinguished with certainty by characters of the male genitalia. Hence, correct species identification and conclusions on distribution and vector status are very difficult and often neglected. Therefore, we developed a reliable and simple mitochondrial cytochrome c oxidase subunit I (COI) gene restriction enzyme assay to discriminate between Cx. pipiens and Cx. torrentium, based on the analysis of morphologically identified male specimens. We sequenced approximately 830 bp in the 3′ region of the mitochondrial COI gene of 18 morphologically identified males of Cx. pipiens and Cx. torrentium. Two restriction enzymes (FspBI and SspI) that could distinguish between the two species according to species-specific differences in these sequences were chosen. The restriction enzymes were tested on 227 samples from Sweden and verified by sequencing 44 of them. The enzyme FspBI correctly identified all investigated samples; the enzyme SspI identified all samples except one Cx. torrentium. We hope the method and the findings presented here will help to shed light on the true distribution and relative proportions of the two species in Europe.

National Category
Biological Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-219397 (URN)10.1111/j.1365-2915.2010.00871.x (DOI)000277975700006 ()20444079 (PubMedID)
Available from: 2014-02-28 Created: 2014-02-28 Last updated: 2017-12-05Bibliographically approved
2. Geographic distribution and relative abundance of the sibling vector species Culex torrentium and Culex pipiens in Sweden
Open this publication in new window or tab >>Geographic distribution and relative abundance of the sibling vector species Culex torrentium and Culex pipiens in Sweden
2011 (English)In: Vector Borne and Zoonotic Diseases, ISSN 1530-3667, E-ISSN 1557-7759, Vol. 11, no 10, 1383-1389 p.Article in journal (Refereed) Published
Abstract [en]

Culex torrentium and Culex pipiens are sibling species and potential viral vectors that coexist in Europe. Larvae and females of the two species are morphologically almost identical, and reliable identification can only be done on males. To investigate the distribution and relative abundance of the two species in Sweden, we collected Culex larvae from sites spread over the country, identified them as Culex pipiens/torrentium based on morphology, and identified them to species using a recently developed restriction enzyme method. Cx. torrentium was the dominant species (89%, n = 1012) and it occurred in 48 of the 49 sites investigated, and also dominated in most of the study sites. The proportion of Cx. pipiens larvae in relation to Cx. torrentium collected at each site decreased with both increasing latitude and altitude, and the presence of Cx. pipiens decreased with latitude. In addition, Cx. pipiens/torrentium females were sampled with Centres for Disease Control light traps baited with carbon dioxide. The overall country mean was 4.0 Cx. pipiens/torrentium caught per trap night, with decreasing numbers of Cx. pipiens/torrentium caught per trap night with increasing latitude. Thus, the abundance of Cx. pipiens/torrentium decreased, but the proportion Cx. torrentium increased, with increasing latitude. This is the first study that shows the vast dominance of Cx. torrentium over Cx. pipiens in Sweden. The unexpected dominance of Cx. torrentium highlights the importance of distinguishing between the two species in studies of Culex-borne arboviruses in Europe.

Keyword
Abundance, Culex pipiens, Culex torrentium, Distribution, Sindbis virus, Sweden, VectorsWest Nile virus
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-160728 (URN)10.1089/vbz.2011.0630 (DOI)000295870800012 ()
Available from: 2011-11-01 Created: 2011-10-31 Last updated: 2017-12-08
3. The arbovirus vector Culex torrentium is more prevalent than Culex pipiens in northern and central Europe
Open this publication in new window or tab >>The arbovirus vector Culex torrentium is more prevalent than Culex pipiens in northern and central Europe
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2014 (English)In: Medical and Veterinary Entomology, ISSN 0269-283X, E-ISSN 1365-2915, Vol. 28, no 2, 179-186 p.Article in journal (Refereed) Published
Abstract [en]

Two species of arbovirus vector, Culex torrentium and Culex pipiens (Diptera: Culicidae), occur in several European countries, but difficulties in their accurate identification and discrimination have hampered both detailed and large-scale distribution and abundance studies. Using a molecular identification method, we identified to species 2559 larvae of Cx. pipiens/torrentium collected from 138 sites in 13 European countries ranging from Scandinavia to the Mediterranean coast. In addition, samples of 1712 males of Cx. pipiens/torrentium collected at several sites in the Czech Republic were identified to species based on the morphology of their hypopygia. We found that the two species occur together in large areas of Europe, and that Cx. torrentium dominates in northern Europe and Cx. pipiens dominates south of the Alps. The transition in dominance occurs in central Europe, where both species are roughly equally common. There was a strong correlation between the length of the growing season at different sites and occurrences of the two species. As the growing season increases, the proportion and detection of Cx. torrentium decrease, whereas those of Cx. pipiens increase. The present findings have important consequences for the interpretation of the results of studies on major enzootic and link-vectors of mosquito-borne bird-associated viruses (i.e. Sindbis, West Nile and Usutu viruses), especially in central Europe and Scandinavia.

National Category
Biological Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-219402 (URN)10.1111/mve.12024 (DOI)000337572500007 ()
Available from: 2014-02-28 Created: 2014-02-28 Last updated: 2017-12-05Bibliographically approved
4. Trapping biases of Culex torrentium and Culex pipiens revealed by comparison of captures in CDC traps, ovitraps, and gravid traps
Open this publication in new window or tab >>Trapping biases of Culex torrentium and Culex pipiens revealed by comparison of captures in CDC traps, ovitraps, and gravid traps
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2015 (English)In: Journal of Vector Ecology, ISSN 1081-1710, E-ISSN 1948-7134, Vol. 40, no 1, 158-163 p.Article in journal (Refereed) Published
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-231365 (URN)10.1111/jvec.12145 (DOI)000355851400019 ()26047196 (PubMedID)
Available from: 2014-09-23 Created: 2014-09-08 Last updated: 2017-12-05Bibliographically approved
5. Exceptional Sindbis virus infection rate in Swedish Culex torrentium defines its role as a major enzootic vector
Open this publication in new window or tab >>Exceptional Sindbis virus infection rate in Swedish Culex torrentium defines its role as a major enzootic vector
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2015 (English)In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059Article in journal (Refereed) Accepted
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-231372 (URN)
Available from: 2014-09-23 Created: 2014-09-08 Last updated: 2017-12-05Bibliographically approved

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