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The Role of Culex Pipiens Mosquitoes in Transmission of West Nile Virus in Europe Mosquitoes in Transmission of West Nile Virus in Europe Chantal B.F

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The Role of Culex Pipiens Mosquitoes in Transmission of West Nile Virus in Europe Mosquitoes in Transmission of West Nile Virus in Europe Chantal B.F The role of Culex pipiens The role of Culex pipiens mosquitoes in transmission of West Nile virus in Europe mosquitoes in transmission of West Nile virus in Europe Chantal B.F. Vogels Nile virus in Europe Chantal B.F. mosquitoes in transmission of West Chantal B.F. Vogels 2017 Propositions 1. Northern Europe must prepare for West Nile virus transmission. (this thesis) 2. West Nile virus can affect the brain of both its vertebrate host and mosquito vector. (this thesis) 3. Conformism is a poor evolutionary strategy. 4. The individual-based character of the scientific review process makes publishing a lottery. 5. Sufficient sleep is key to a successful career. 6. Benefits of doing sports outweigh the risks of injury. Propositions belonging to the thesis, entitled ‘The role of Culex pipiens mosquitoes in transmission of West Nile virus in Europe’ Chantal B.F. Vogels Wageningen, 8 September 2017 The role of Culex pipiens mosquitoes in transmission of West Nile virus in Europe Chantal B.F. Vogels Thesis committee Promotor Prof. Dr M. Dicke Professor of Entomology Wageningen University & Research Co-promotor Dr C.J.M. Koenraadt Assistant professor, Laboratory of Entomology Wageningen University & Research Other members Prof. Dr R.A.A. van der Vlugt, Wageningen University & Research Dr M.A.H. Braks, National Institute for Public Health and the Environment, Bilthoven Dr L.S. van Overbeek, Wageningen University & Research Dr W.F. de Boer, Wageningen University & Research This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation The role of Culex pipiens mosquitoes in transmission of West Nile virus in Europe Chantal B.F. Vogels Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 8 September 2017 at 4 p.m. in the Aula. Chantal B.F. Vogels The role of Culex pipiens mosquitoes in transmission of West Nile virus in Europe, 212 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2017) With references, with summaries in English and Dutch ISBN 978-94-6343-615-1 DOI http://dx.doi.org/10.18174/418217 Table of contents Abstract 9 Chapter 1 11 Introduction Chapter 2 23 Winter activity and aboveground hybridization between the two biotypes of the West Nile virus vector Culex pipiens Chapter 3 37 Latitudinal diversity of Culex pipiens biotypes and hybrids in farm, peri-urban, and wetland habitats in Europe Chapter 4 51 Vector competence of northern European Culex pipiens biotypes and hybrids for West Nile virus is differentially affected by temperature Chapter 5 65 Vector competence of northern and southern European Culex pipiens pipiens mosquitoes for West Nile virus across a gradient of temperatures Chapter 6 79 Virus interferes with host-seeking behaviour of mosquito Chapter 7 95 Modelling West Nile virus transmission risk in Europe: effect of temperature and mosquito biotypes on the basic reproduction number Chapter 8 115 Vector competence of European mosquitoes for West Nile virus Chapter 9 143 General discussion: Identification of mosquito-related factors that limit West Nile virus transmission in northern Europe References 161 Summary 183 Samenvatting 189 Acknowledgements 195 Curriculum vitae 201 List of publications 205 Training and education statement 209 Abstract 8 Abstract West Nile virus (WNV) is maintained in a natural transmission cycle between mosquito vectors and bird hosts. However, mosquitoes can also transmit WNV to mammals, such as humans and horses, which may result in disease. In Europe, such cases of WNV disease are yearly recurring in southern and central Europe, but have not been detected in northern Europe. The absence of WNV outbreaks in northern Europe may be explained by lowered vector competence of the main vector for WNV: the northern house mosquito, Culex (Cx.) pipiens. The aim of this thesis was, therefore, to investigate the role of Cx. pipiens mosquitoes in transmission of WNV in Europe, in order to understand differences in WNV circulation between northern and southern Europe. The species Cx. pipiens consists of two biotypes, pipiens and molestus, which can form hybrids. Both biotypes and their hybrids are morphologically identical but differ in their behaviour, which may have consequences for WNV transmission. In this thesis, the Cx. pipiens biotype composition was investigated in The Netherlands, and more broadly at the European scale. These studies revealed that both biotypes and their hybrids are present throughout The Netherlands, and that there is a shift towards relatively more biotype pipiens mosquitoes at northern latitudes in Europe. The next step was to assess vector competence of these northern European biotypes and their hybrids, and to make a direct comparison with vector competence of a southern European population. Both biotypes and their hybrids originating from The Netherlands are competent vectors for WNV. Interestingly, no differences in vector competence were found between a Dutch and Italian biotype pipiens population. However, both studies revealed that low temperatures of 18 °C are an important limiting factor for WNV transmission. A more in-depth study on the effects of WNV on the host-seeking behaviour of biotype pipiens mosquitoes revealed that WNV infection reduces the host-seeking response towards host odour, but that other fitness parameters (e.g. flight activity, blood-feeding, and survival) are not affected. When results from the biotype composition and vector competence studies were included in a newly developed R0 model, it becomes clear that biotype pipiens is the main contributor to WNV transmission. The results presented in this thesis show that the Cx. pipiens biotypes and their hybrids are present throughout The Netherlands, and that they can transmit WNV under favourable climatic conditions. The absence of WNV outbreaks in northern Europe can most likely be explained by low temperature which has a negative effect on mosquito abundance, vector competence, and the duration of the infectious period. When considering the outcomes of this thesis in the light of climate change, northern European countries such as The Netherlands should be prepared for future WNV transmission. 8 9 Chapter 1 Introduction Chapter 1 Emerging arthropod-borne viruses Arthropod-borne (arbo)viruses deploy a fascinating evolutionary strategy, by alternating replication in vertebrate and invertebrate hosts (Weaver 2006). As a consequence, most arboviruses have complex transmission cycles involving arthropod vectors, which transmit the virus from one vertebrate host to another 1 (Weaver & Barrett 2004). Transmission cycles can only be established under suitable climatic conditions, because virus replication is influenced by temperature (Hardy et al. 1983). Mosquitoes are one of the most important vectors for arboviruses of medical and veterinary importance. The majority of medically important arboviruses transmitted by mosquitoes, such as dengue, chikungunya, and Zika virus, are circulating in the tropics (Weaver & Reisen 2010). However, globalisation and climate change have contributed to the emergence of arboviruses in more temperate regions, including Europe (Kilpatrick & Randolph 2012, Morse 1995). During the past decades several mosquito-borne viruses have been introduced in Europe, causing diseases in humans (Calistri et al. 2010a, Tomasello & Schlagenhauf 2013). Of these viruses, West Nile virus (WNV; family: Flaviviridae) can be considered the mosquito-borne virus of highest medical and veterinary importance for Europe, due to the recurrent number of cases in humans and equines every summer (ECDC 2016). WNV is most notorious for its rapid spread throughout the United States of America (USA; Hayes et al. 2005). Since the introduction in New York in 1999, WNV spread from the East to the West coast within 5 years (Hayes et al. 2005). In contrast, such rapid spread has not been observed in Europe, where cases of WNV in humans have been limited to southern and central European countries (Figure 1; ECDC 2016). Thus far, no cases of WNV in humans have been reported in northern Europe. Differences in WNV circulation between northern and southern Europe may possibly be explained by host-related, vector-related, and environmental factors, or the interaction between these factors. The aim of this thesis was to investigate the role of mosquitoes in transmission of WNV in Europe, in order to understand differences in WNV circulation between northern and southern Europe. West Nile virus WNV is maintained in a natural transmission cycle between birds and mosquitoes (Figure 2). Mosquitoes can transmit WNV to mammals, including humans and equines, which may result in disease. However, in general mammals do not develop high enough virus levels in their blood (viraemia) to support further transmission to mosquitoes (Hayes et al. 2005). Therefore, they are considered “dead-end” hosts. An estimated 80 percent of human infections with WNV remain asymptomatic, and, thus, many WNV cases remain undetected or unreported. Symptomatic cases 12 Introduction mostly develop into fever and less than 1 percent of cases develops neurological disease, such as encephalitis (Mostashari et al. 2001). Currently, there is no vaccine or specific treatment against WNV available for humans. From 1999 to 2016, over 46,000 cases of WNV human disease, and approximately 2,000 deaths have been reported in the USA (CDC 2015). In contrast, a few hundred human disease cases are yearly reported in Europe (ECDC 2016). 1 Figure 1: European countries with reported cases of West Nile virus infection in humans. Countries marked in grey have experienced human cases of West Nile virus since 2010. Countries marked in white have not reported any cases of West Nile virus in humans. Dataset provided by ECDC, based on data provided by WHO and Ministries of Health from the affected countries (ECDC 2016). WNV was discovered for the first time in Uganda in 1937 (Smithburn et al.
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