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1 UNIVERSITÀ DEGLI STUDI DI MILANO SCUOLA DI DOTTORATO Terra Ambiente E Biodiversità Dipartimento Di Scienze Veterinarie E

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1 UNIVERSITÀ DEGLI STUDI DI MILANO SCUOLA DI DOTTORATO Terra Ambiente E Biodiversità Dipartimento Di Scienze Veterinarie E UNIVERSITÀ DEGLI STUDI DI MILANO SCUOLA DI DOTTORATO Terra Ambiente e Biodiversità Dipartimento di Scienze veterinarie e sanità pubblica - DIVET- Dottorato di Ricerca in Biologia Animale, XXV Ciclo Hard ticks (ACARINA , IXODIDAE ): species identification, phylogeny and symbioses - VET/06 ─ BIO/05 - MATTEO MONTAGNA Tutore prof. CLAUDIO BANDI Coordinatore del Dottorato prof. MARCO FERRAGUTI 2011-2012 1 Statement to my Thesis This work was carried out in the group of Prof. Claudio Bandi at the Università degli Studi di Milano. My PhD thesis committee consisted of: Prof. GIORGIO BAVESTRELLO Prof. CLAUDIO BANDI Dott.sa MARIA GABRIELLA MARIN My thesis is written in a cumulative format. It consists of a synopsis covering several aspects concerning to my research works on ticks (Acarina, Ixodidae) with a global approach, from morphological/molecular taxonomy to bacteria harbored and transmitted by ticks, to genomic, expression and population genetic studies. This is followed by result chapters presenting my research consisting of four published research article, a submitted manuscript, an accepted manuscript and one manuscript in preparation. Finally, I have reported other aspect of my research work during my phD experience (i.e. other published papers, research activities and grants received). 2 1. Introduction and aim of the thesis 6 1.1 References 10 2. Results 13 2.1 Research article I: "Evaluation of DNA Barcoding as tool to identify hard ticks (genus AMBLYOMMA Koch 1844, Acarina, Ixodidae)" (manuscript in preparation) 13 2.1.1 Summary 13 2.1.2 Manuscript 13 2.1.3 References 21 2.1.4 Appendix 23 2.2 Research article II: "Screening for bacterial DNA in the hard tick Hyalomma marginatum (Ixodidae) from Socotra Island (Yemen): detection of Francisella-like endosymbiont" (published on Journal of Acarological and Entomological Research) 26 2.2.1 Summary 26 2.2.2 Manuscript 26 2.2.3 References 31 2.3 Research article III: "Phylogenomic evidence for the presence of a flagellum and cbb3 oxidase in the free-living mitochondrial ancestor" (published on Molecular Biology and Evolution) 34 2.3.1 Summary 34 2.3.2 Manuscript 34 2.3.3 References 50 2.3.4 Supplementary materials 56 2.4 Research article IV: "Midichloria and like organisms form an ecologically widespread clade of intracellular alpha-proteobacteria" (manuscript submitted to Applied and Environmental Microbiology) 61 2.4.1 Summary 61 2.4.2 Manuscript 61 2.4.3 References 76 3 2.5 Research article IV: "Tick-Box for 3'-end formation of mitochondrial transcripts in Ixodida, basal chelicerates and DROSOPHILA " (published on PlosOne) 80 2.5.1 Summary 80 2.5.2 Manuscript 80 2.5.3 References 104 2.5.4 Supplementary materials 110 2.6 Research article V: "Localization of the bacterial symbiont Candidatus Midichloria mitochondrii within the hard tick Ixodes ricinus by whole-mount FISH staining" (published on Ticks and Tick-Borne Diseases) 119 2.6.1 Summary 119 2.6.2 Manuscript 119 2.6.3 References 132 2.7 Research article VII: "Multiple independent data reveals an unusual response to Pleistocene climatic changes in the hard tick IXODES RICINUS " (accepted on Molecular Ecology) 135 2.7.1 Summary 135 2.7.2 Manuscript 135 2.7.3 References 156 2.7.4 Appendix 165 3. Other relevant publications produced during my phD (a color version of the pdf documents are stored in a separate folder on CD-ROM attached to the printed copy) 167 3.1 Research article: "PACHYBRACHIS SASSII , a new species from the Mediterranean Giglio Island (Italy) (Coleoptera, Chrysomelidae, Cryptocephalinae). ZooKeys (2011), 155: 51–60" 167 3.2 Research article: "Molecular Evidence for Multiple Infections as Revealed by Typing of ASAIA Bacterial Symbionts of Four Mosquito Species. Applied and Environmental Microbiology (2010), 76(22): 7444–7450" 167 4 3.3 Research article: "The Beetle (Coleoptera) and True bug (Heteroptera) species pool of the Alpine "Pian di Gembro" wetland (Villa di Tirano, Italy) and its conservation. Journal of Entomological and Acarological Research (2011) 43: 7-22" 167 3.4 Research article: "Insect community structure and insect biodiversity conservation in an Alpine wetland subjected to an intermediate diversified management regime. Ecological Engineering (2012), 47: 242–246" 167 3.5 Research article: "Molecular typing of bacteria of the genus ASAIA in malaria vector ANOPHELES ARABIENSIS Patton, 1905. Journal of Entomological and Acarological Research (2012) 44: 33-36" 167 3.6 Research article: "A study on the presence of flagella in the order Rickettsiales: the case of ‘Candidatus Midichloria mitochondrii’. Microbiology (2012), 158, 1677–1683" 167 4 Grants and projects 168 5 Curriculum vitae 223 5 1 Introduction and aim of the thesis Ticks (Acari, Parasitiformes, Ixodida) are obligate blood-sucking ectoparasites able to parasitize a great variety of terrestrial vertebrates (mammals, birds, reptiles and amphibians) (Sonenshine 1991, 1993). Fossil members of the Parasitiformes appear in the late Cretaceous, 100.5 - 66 Mya (Poinar and Brown 2003), but the ancestor of ticks evolved probably in pre-mid Cretaceous period, 145 - 120 Mya (Klompen et al. 1996; Nava et al. 2009). The primary hosts may have been reptiles or amphibians (Nava et al. 2009), but the major adaptive radiation probably occurred in mid-Cenozoic following the radiation of their hosts (Poinar 1995; Klompen et al. 1996). Nowadays approximately 870 species of ticks are described (Horak et al. 2002; Keirans 2009) and are subdivided into three families: Argasidae, or soft ticks because of the lack of a sclerotized dorsal scutum, and with the capitulum positioned ventrally; Ixodidae (or hard ticks) possess a sclerotized dorsal scutum and an apical positioned capitulum; the monotypic family of Nuttalliellidae, in which Nuttaliella namaqua Bedford, 1931 shows features of both hard and soft ticks, in fact it possess a partly sclerotized pseudo-scutum and an apical positioned capitulum (Keirans et al. 1976; El Shoura 1990). Ixodidae can be divided in two morphological groups on the basis of the anal groove position, the prostriata (including only the genus Ixodes ) are considered the basal lineage and they possess the anal groove anteriorly to the anus; the metastriata (including all the other 11 genera) possess the anal groove posteriorly to the anus (Nava et al. 2009). Phylogenetic analyses based both on morphological (using up to 125 characters) and molecular characters (using different markers, the nuclear 18S rRNA and 28S rRNA genes, and the mitochondrial 12S rRNA and 16S rRNA genes and the 11 concatenated mitochondrial protein coding genes) agree in considering the tick clade as monophyletic (Klompen et al. 2000; Xu et al. 2003; Jayeprakash & Hoy 2009; Mans et al. 2011; Burger et al. 2012). Phylogenetic relationships among the three families remained unresolved until the recent work of Mans and colleagues (2011) that collected alive specimens of N. namaqua (Nuttalliellidae). The analyses based on the nuclear gene 18S rRNA for different parasitiformes species highlighted as basal the branch leading to N. namaqua indicating that the common ancestor shares features of both soft and hard ticks (Mans et al. 2011). Excluding mosquitoes, able to transmit different species of Plasmodium (Apicomplexa), filarial nematodes and a variety of viruses, ticks are nowadays considered the most important group of arthropod vectors, capable of transmitting a variety of pathogens vertebrate animals including humans (Jongejan & Uilenberg 2004). Microorganisms such as bacteria (e.g. Rickettsia spp., Borrelia burgdorferi sensu lato, Erlichia spp. and Francisella spp.), protozoa (e.g. Babesia spp.) and viruses (like Crimean-Congo hemorrhagic fever, Tick Borne Encephalitis) can be transmitted to 6 the host as a result of a tick bite (Sonenshine 1991; Parola & Raoult 2001; Jongejan & Uilenberg 2004). In the last decades the scenarios become even more serious as result of the climate change and as a consequence, ticks expanded their distributional range especially towards higher altitudes and latitudes with the spreading of the transmitted pathogens even in highly populated environments (Lindgren et al. 2000; Cumming 2002; Danielova et al. 2006; Hubálek 2009; Pistone et al. 2011). Furthermore ticks can play an important role as reservoirs of these bacteria in nature (Parola & Raoult, 2001). In Europe and North America the Lyme disease, caused by the pathogenic Borrelia burgdorferi sensu lato and transmitted respectively by Ixodes ricinus (Linnaeus, 1758) and Ixodes scapularis Say, 1821, is the most prevalent arthropod-born disease (Rizzoli et al. 2011; Wright et al. 2012). In Europe every years approximately 65.500 people suffer of Lyme disease symptoms (Hubálek 2009). The medical diagnosis of Lyme diseases (and in general of tick-borne diseases) could be intricate and only the appearance of erythema migrans rash could be decisive for the Lyme diagnosis in absence of laboratory analysis, that are anyway not always conclusive (Wright et al. 2012). In fact after the clinical examination and the patient anamnesis, the used laboratory diagnostic protocols involve blood sampling and serological analysis for indirect diagnosis; serological analysis requires the seroconversion time, and can thus be effected after no less than 6 weeks after the tick bite. This last feature associated with the fact that tick-borne pathogens are generally highly specific for a given tick genus (e.g. the etiological agent of the Lyme disease, Borrelia burgdorferi , can be transmitted only by the ticks of the genus Ixodes ) highlight the needs on one hand to perform a PCR screening on the tick sample in order to evaluate the presence of pathogens, and on the other to correctly identify the tick taxon, even starting from a fraction of the whole organism obtained from patients that had not been properly preserved. Identification of tick samples based on morphology requires experience and a high level of knowledge of these arthropods, furthermore most discriminating morphological features are sometimes visible only in adult specimens, making species identification of immature stages not always possible.
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