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Evolution and ecology of Drosophila sigma viruses

Insects are host to a diverse range of vertically transmitted micro-organisms, but while their bacterial symbionts are well-studied, little is known about their vertically transmitted viruses. The sigma virus (DMelSV) is currently the only natural hostspecific pathogen to be described in Drosophila melanogaster. In this thesis I have examined; the diversity and evolution of sigma viruses in Drosophila, their transmission and population dynamics, and their ability to host shift. I have described six new rhabdoviruses in five Drosophila species — D. affinis, D. obscura, D. tristis, D. immigrans and D. ananassae — and one in a member of the Muscidae, Muscina stabulans (Chapters two and four). These viruses have been tentatively named as DAffSV, DObsSV, DTriSV, DImmSV, DAnaSV and MStaSV respectively. I sequenced the complete genomes of DObsSV and DMelSV, the L gene from DAffSV and partial L gene sequences from the other viruses. Using this new sequence data I created a phylogeny of the rhabdoviruses (Chapter two). The sigma viruses form a distinct clade which is closely related to the Dimarhabdovirus supergroup, and the high levels of divergence between these viruses suggest that they may deserve to be recognised as a new genus. Furthermore, this analysis produced the most robustly supported phylogeny of the Rhabdoviridae to date, allowing me to reconstruct the major transitions that have occurred during the evolution of the family. This data suggests that the bias towards research into plants and vertebrates means that much of the diversity of rhabdoviruses has been missed, and rhabdoviruses may be common pathogens of insects. In Chapter three I examined whether the new sigma viruses in Drosophila affinis and Drosophila obscura are both vertically transmitted. As is the case for DMelSV, both males and females can transmit these viruses to their offspring. Males transmit lower viral titres through sperm than females transmit through eggs, and a lower proportion of their offspring become infected. I then examined natural populations of D. obscura in the UK; 39% of flies were infected and the viral population shows clear evidence of a recent expansion, with extremely low genetic diversity and a large excess of rare polymorphisms. Using sequence data I estimate that the virus has swept across the UK within the last ~11 years, during which time the viral population size doubled approximately every 9 months. Using simulations based on lab estimates of transmission rates, I show that the biparental mode of transmission allows the virus to invade and rapidly spread through populations, at rates consistent with those measured in the field. Therefore, as predicted by the simulations, the virus has undergone an extremely rapid and recent increase in population size. In Chapter four I investigated for the first time whether vertically transmitted viruses undergo host shifts or cospeciate with their hosts. Using a phylogenetic approach I show that sigma viruses have switched between hosts during their evolutionary history. These results suggest that sigma virus infections may be short-lived in a given host lineage, so that their long-term persistence relies on rare horizontal transmission events between hosts. In Chapter five I examined the ability of three Drosophila sigma viruses to persist and replicate in 51 hosts sampled across the Drosophilidae phylogeny. I used a phylogenetic mixed model to account for the non-independence of host taxa due to common ancestry, which additionally allows integration over the uncertainty in the host phylogeny. In two out of the three viruses there was a negative correlation between viral titre and genetic distance from the natural host. Additionally the host phylogeny explains an extremely high proportion of the variation (after considering genetic distance from the natural host) in the ability of these viruses to replicate in novel hosts (>0.8 for all viruses). There were strong phylogenetic correlations between all the viruses (>0.65 for all pairs), suggesting a given species’ level of resistance to one virus is strongly correlated with its resistance to other viruses. This suggests the host phylogeny, and genetic distance from the natural host, may be important in determining viruses ability to host switch. This work has aimed to address fundamental questions relating to host-parasite coevolution and pathogen emergence. The data presented suggests that sigma viruses are likely to be widespread vertically transmitted insect viruses, which have dynamic interactions with their hosts. These viruses appear to have switched between hosts during their evolutionary history and it is likely the host phylogeny is a determinant of such host shifts.

Identiferoai:union.ndltd.org:bl.uk/oai:ethos.bl.uk:563628
Date January 2011
CreatorsLongdon, Ben John
ContributorsObbard, Darren. ; Little, Thomas. ; Jiggins, Francis
PublisherUniversity of Edinburgh
Source SetsEthos UK
Detected LanguageEnglish
TypeElectronic Thesis or Dissertation
Sourcehttp://hdl.handle.net/1842/5768

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