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Culex Pipiens Universidade Nova de Lisboa Instituto de Higiene e Medicina Tropical Genetic studies on the mosquito vector Culex pipiens . Bruno Gomes da Silva Licenciado em Biologia da Universidade do Porto Dissertação apresentada para cumprimento dos requisitos necessários à obtenção do grau de Doutor no Ramo de Ciências Biomédicas, Especialidade em Parasitologia, realizada sob orientação científica do Prof. Dr. João Pinto. Orientador : Prof. Dr. João Pinto Unidade de Parasitologia Médica Instituto de Higiene e Medicina Tropical Co-orientadores: Prof. Dr. António P.G. Almeida Unidade de Parasitologia Médica Instituto de Higiene e Medicina Tropical Prof. Dr. Martin J. Donnelly Department of Vector Biology Liverpool School of Tropical Medicine Comissão Tutorial : Prof. Dr. Henrique Silveira Unidade de Parasitologia Médica Instituto de Higiene e Medicina Tropical O trabalho foi financiado pela Fundação para a Ciência e Tecnologia, através da bolsa de doutoramento SFRH/BD/36410/2007 e dos projectos de investigação POCI/BIA-BDE/57650/2004 e PPCDT/BIA-BDE/57650/2004. JANEIRO , 2013 ii Para o casal que me deu a fala, E o tradutor que me ligou ao Mundo. iii Acknowledgements Firstly, I would like to acknowledge to my colleagues at IHMT and LSTM. My sincerely thanks to João Pinto, my supervisor, for his knowledge, enthusiasm and patience, which were welcome and essential in helping me to complete this project and thesis. Martin J. Donnelly, my co-supervisor, provided support and advice during the period I spent at Liverpool School of Tropical Medicine and I appreciate his enthusiasm in the development of this project. António P. G. Almeida, my co-supervisor, provided essential support in the field and in the ecological perspectives of the thesis. Carla A. Sousa, Patricia Salgueiro and José L. Vicente were essential partners during the last four years to perform several tasks in the laboratory and field at IHMT during the last four years. Craig Wilding, David Weetman and Keith Steen supported the development of the laboratory and molecular analysis performed at LSTM. Other colleagues from the IHMT, Ana R. Côrte-Real, Eliane Arez, Ferdinando B. Freitas, Inês Vieira, Isabel Calderón, Joana Alves, Leonor Pinho, Maria T. Freitas, Ricardo Alves and Teresa L. Silva also provided valuable assistance in this project. I would like to thank Harry Savage (Centers for Disease Control and Prevention, USA), John Vontas (University of Crete, Greece) and Marta Santa-Ana (University of Madeira, Portugal), for field work support and providing mosquito samples. Also, thanks to Deirdre Walshe and Teresa L. Silva for proofreading this thesis. I would like to acknowledge the administrative support from the Departments of Entomology, Malaria, and Parasitology at IHMT and Vector Biology at LSTM. This study was funded by a PhD fellowship from the Fundação para a Ciência e Tecnologia/MCTES (SFRH/BD/36410/2007) and by projects of the Fundação para a Ciência e a Tecnologia, Portugal (POCI/BIA-BDE/57650/2004 and PPCDT/BIA- BDE/57650/2004). Last but by no means least, thank you to all of my family and friends who helped me to grown as a person, especially my parents and my big brother. The moments that we spent together, from calm conversations to noisy moments, helped me to maintain my sanity over the past four years. iv Resumo As duas espécies do complexo Culex pipiens com maior distribuição geográfica, Culex quinquefasciatus e Culex pipiens sensu stricto, são importantes vectores de filárias e arbovírus. Culex pipiens s.s. apresenta categorias intra-específicas definidas por características ecológicas e fisiológicas, das quais as formas pipiens e molestus têm sido implicadas na transmissão do vírus da Febre do Nilo Ocidental na Europa e América do Norte. Hibridação entre Cx. quinquefasciatus e Cx. pipiens s.s. foi documentada em algumas regiões geográficas onde ambas espécies coexistem simpatricamente. Este fenómeno também foi descrito entre as formas molestus e pipiens, em áreas de simpatria e quando existe contacto limitado em certas épocas do ano. No entanto, o impacto da hibridação na divergência genética entre as espécies ou formas está por clarificar. Além disso, a hibridação pode afectar características ecológicas/fisiológicas das espécies/formas, que podem influenciar a sua capacidade vectorial. Neste contexto, foram analisadas populações do complexo Cx. pipiens da Europa, EUA e da Macaronésia com objectivo de determinar níveis de diferenciação genética e taxas de hibridação entre os membros do complexo. As amostras de mosquitos foram obtidas por diferentes métodos de colheita no terreno e a partir de colónias laboratoriais, entre 2005 e 2011. As análises genéticas realizadas foram baseadas em microssatélites e por polimorfismos de comprimento de fragmentos amplificados . Foram efectuadas comparações abordando questões específicas a diferentes níveis taxonómicos, que estão descritas nos cinco capítulos de resultados da tese. A distribuição e níveis de hibridação entre Cx. quinquefasciatus e Cx. pipiens s.s. foram avaliados nas ilhas da Macaronésia, o que permitiu detectar híbridos (~40%) em duas ilhas do arquipélago de Cabo Verde. A distribuição destas espécies na região reflecte a biogeografia e aspectos históricos da colonização humana. A coexistência em habitats de superfície das formas molestus e pipiens na região da Comporta (Portugal), foi demostrada pela combinação de análises fenotípicas e genéticas. As análises moleculares também sugerem a existência de um padrão de introgressão assimétrica, de molestus para pipiens. Estudos adicionais, sugerem uma v maior tendência da forma molestus para explorar habitats intradomiciliares/antropogénicos quando comparada com a forma pipiens. Em ambas as formas, mais de 90% das refeições sanguíneas foram realizadas em aves. Foi ainda efectuada a primeira análise genómica focada na divergência entre os genomas das formas molestus e pipiens. Esta análise indicou uma baixa divergência entre os dois genomas (1,4%–3,1%), o que é consistente com um processo de especiação simpátrica com fluxo génico. Finalmente, foram realizadas análises genéticas em amostras de Cx. pipiens s.s. colhidas na Grécia durante um surto de Febre do Nilo Ocidental, em 2010. Populações simpátricas de molestus e pipiens com introgressão assimétrica foram identificadas na região onde o surto ocorreu, enquanto uma população homogénea de molestus foi encontrada numa região sem transmissão do vírus. Estes resultados evidenciam a importância da caracterização da variação genética e das relações evolutivas entre os membros do complexo Cx. pipiens para entender o seu potencial como vectores de doenças. Também abrem novas perspectivas para a investigação da ecologia e evolução deste complexo de espécies com importância médica. PALAVRAS -CHAVE : Culex pipiens, Culex quinquefasciatus, molestus, genética populacional, hibridação, especiação com fluxo génico, vírus de Febre do Nilo. vi Abstract The two widespread species of the Culex pipiens complex, Culex quinquefasciatus and Culex pipiens sensu stricto , are major vectors of filarial worms and arboviruses. Culex pipiens s.s. is also divided into intraspecific categories defined by ecological and physiological traits. Of these, two forms, denoted pipiens and molestus, have been implicated in West Nile virus transmission in Europe and North America. Inter-specific hybridisation between Cx. quinquefasciatus and Cx. pipiens s.s. has been documented in some geographic regions where both species occur sympatrically. Likewise, hybridisation between molestus and pipiens forms has been described in areas of sympatry or when the forms become in contact during certain times of the year. However, the impact of hybridisation on the extent of genetic divergence between species or forms remains uncertain. Moreover, hybridisation may affect ecological and physiological traits of the species/forms, which may influence their vectorial capacity. In this context, the degree of genetic differentiation and hybridisation between members of the Cx. pipiens complex was studied in populations from Europe, USA and Macaronesian islands. Mosquito samples were obtained from field collections or laboratory colonies between 2005 and 2011. Genetic analyses were based on microsatellite genotypes and amplified fragment length polymorphisms. Comparisons were made at different taxonomic levels, addressing specific questions. These are described in the five results chapters of this thesis. The distribution and hybridisation between Cx. quinquefasciatus and Cx. pipiens s.s. were assessed in Macaronesian islands. Hybrid rates ~40% were detected in two islands of the Cape Verde archipelago. The distribution of the species reflects both the islands' biogeography and historical aspects of human colonization. A combination of phenotypic and genetic analyses conducted in Comporta (Portugal) revealed the co-occurrence of molestus and pipiens forms of Cx. pipiens s.s. in aboveground habitats. Moreover, a pattern of asymmetric introgression from molestus into pipiens was found. Subsequent molecular and ecological analyses carried out in the same region suggested that the molestus form has a higher tendency to vii explore indoor/anthropogenic habitats, when compared with the sympatric pipiens form. In both forms, over 90% of blood meals were made on avian hosts. The first genomic scan addressing levels of genome divergence between molestus and pipiens forms was implemented. Low levels of inter-form genomic divergence (1.4%–3.1%) were detected, consistent with
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