Rhabdoviruses in Two Species of Drosophila: Vertical Transmission and a Recent Sweep

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. We have found that two sigma viruses (Rhabdoviridae) recently discovered in Drosophila affinis and Drosophila obscura are both vertically transmitted. As is the case for the sigma virus of Drosophila melanogaster, we find that both males and females can transmit these viruses to their offspring. Males transmit lower viral titers through sperm than females transmit through eggs, and a lower proportion of their offspring become infected. In natural populations of D. obscura in the United Kingdom, we found that 39% of flies were infected and that 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 we estimate that the virus has swept across the United Kingdom within the past ∼11 years, during which time the viral population size doubled approximately every 9 months. Using simulations based on our lab estimates of transmission rates, we 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 our simulations, the virus has undergone an extremely rapid and recent increase in population size. In light of this and earlier studies of a related virus in D. melanogaster, we conclude that vertically transmitted rhabdoviruses may be common in insects and that these host–parasite interactions can be highly dynamic

Disease association mapping in Drosophila can be replicated in the wild

Association and linkage mapping have become important tools in understanding the genetics of complex traits, including diseases in humans. As the success of association mapping is reduced by small effect sizes and limited power, linkage studies in laboratory-based model systems are still heavily used. But whether the results of these studies can be replicated in natural populations has been questioned. Here, we show that a polymorphism in the gene ref(2)P, which had previously been linked to sigma virus resistance in Drosophila melanogaster under laboratory conditions, also provides resistance against the virus in female flies in a wild population in the field. This genetic association is thus upheld in spite of a known genotype-by-genotype interaction and environmental variation

Successive Increases in the Resistance of Drosophila to Viral Infection through a Transposon Insertion Followed by a Duplication

To understand the molecular basis of how hosts evolve resistance to their parasites, we have investigated the genes that cause variation in the susceptibility of Drosophila melanogaster to viral infection. Using a host-specific pathogen of D. melanogaster called the sigma virus (Rhabdoviridae), we mapped a major-effect polymorphism to a region containing two paralogous genes called CHKov1 and CHKov2. In a panel of inbred fly lines, we found that a transposable element insertion in the protein coding sequence of CHKov1 is associated with increased resistance to infection. Previous research has shown that this insertion results in a truncated messenger RNA that encodes a far shorter protein than the susceptible allele. This resistant allele has rapidly increased in frequency under directional selection and is now the commonest form of the gene in natural populations. Using genetic mapping and site-specific recombination, we identified a third genotype with considerably greater resistance that is currently rare in the wild. In these flies there have been two duplications, resulting in three copies of both the truncated allele of CHKov1 and CHKov2 (one of which is also truncated). Remarkably, the truncated allele of CHKov1 has previously been found to confer resistance to organophosphate insecticides. As estimates of the age of this allele predate the use of insecticides, it is likely that this allele initially functioned as a defence against viruses and fortuitously “pre-adapted” flies to insecticides. These results demonstrate that strong selection by parasites for increased host resistance can result in major genetic changes and rapid shifts in allele frequencies; and, contrary to the prevailing view that resistance to pathogens can be a costly trait to evolve, the pleiotropic effects of these changes can have unexpected benefits

The Transcriptional Response of Drosophila melanogaster to Infection with the Sigma Virus (Rhabdoviridae)

Bacterial and fungal infections induce a potent immune response in Drosophila melanogaster, but it is unclear whether viral infections induce an antiviral immune response. Using microarrays, we examined the changes in gene expression in Drosophila that occur in response to infection with the sigma virus, a negative-stranded RNA virus (Rhabdoviridae) that occurs in wild populations of D. melanogaster. We detected many changes in gene expression in infected flies, but found no evidence for the activation of the Toll, IMD or Jak-STAT pathways, which control immune responses against bacteria and fungi. We identified a number of functional categories of genes, including serine proteases, ribosomal proteins and chorion proteins that were overrepresented among the differentially expressed genes. We also found that the sigma virus alters the expression of many more genes in males than in females. These data suggest that either Drosophila do not mount an immune response against the sigma virus, or that the immune response is not controlled by known immune pathways. If the latter is true, the genes that we identified as differentially expressed after infection are promising candidates for controlling the host's response to the sigma virus