Male-killing bacteria in insects: mechanisms, incidence and implications

Bacteria that are vertically transmitted through female hosts and kill male hosts that inherit them were first recorded in insects during the 1950s. Recent studies have shown these "male-killers" to be diverse and have led to a reappraisal of the biology of many groups of bacteria. Rickettsia, for instance, have been regarded as human pathogens transmitted by arthropods. The finding of a male-killing Rickettsia obligately associated with an insect suggests that the genus' members may be primarily associated with arthropods and are only sometimes pathogens of vertebrates. We examined both how killing of male hosts affects the dynamics of inherited bacteria and how male-killing bacteria affect their host populations. Finally, we assessed the potential use of these microorganisms in the control of insect populations

Flies on the move: an inherited virus mirrors Drosophila melanogaster's elusive ecology and demography.

Journal ArticleResearch Support, Non-U.S. Gov'tCopyright © 2014 John Wiley & Sons LtdThis is the accepted version of the following article: Wilfert, L. and Jiggins, F. M. (2014), Flies on the move: an inherited virus mirrors Drosophila melanogaster's elusive ecology and demography. Molecular Ecology, 23: 2093–2104. doi: 10.1111/mec.12709, which has been published in final form at http://onlinelibrary.wiley.com/doi/10.1111/mec.12709/abstractVertically transmitted parasites rely on their host's reproduction for their transmission, leading to the evolutionary histories of both parties being intimately entwined. Parasites can thus serve as a population genetic magnifying glass for their host's demographic history. Here, we study the fruitfly Drosophila melanogaster's vertically transmitted sigma virus DMelSV. The virus has a high mutation rate and low effective population size, allowing us to reconstruct at a fine scale how the combined forces of the movement of flies and selection on the virus have shaped its migration patterns. We found that the virus is likely to have spread to Europe from Africa, mirroring the colonization route of Drosophila. The North American DMelSV population appears to be the result of a recent single immigration from Europe, invading together with its host in the late 19th century. Across Europe, DMelSV migration rates are low and populations are highly genetically structured, likely reflecting limited fly movement. Despite being intolerant of extreme cold, viral diversity suggests that fly populations can persist in harsh continental climates and that recolonization from the warmer south plays a minor role. In conclusion, studying DMelSV can provide insights into the poorly understood ecology of D. melanogaster, one of the best-studied organisms in biology.Leverhulme TrustRoyal Society University Research Fellowshi

Latitudinal clines in gene expression and cis\textit{cis}-regulatory element variation in Drosophila melanogaster\textit{Drosophila melanogaster}

$\textbf{BACKGROUND}$: Organisms can rapidly adapt to their environment when colonizing a new habitat, and this could occur by changing protein sequences or by altering patterns of gene expression. The importance of gene expression in driving local adaptation is increasingly being appreciated, and $\textit{cis}$-regulatory elements (CREs), which control and modify the expression of the nearby genes, are predicted to play an important role. Here we investigate genetic variation in gene expression in immune-challenged $\textit{Drosophila melanogaster}$ from temperate and tropical or sub-tropical populations in Australia and United States. $\textbf{RESULTS}$: We find parallel latitudinal changes in gene expression, with genes involved in immunity, insecticide resistance, reproduction, and the response to the environment being especially likely to differ between latitudes. By measuring allele-specific gene expression (ASE), we show that $\textit{cis}$-regulatory variation also shows parallel latitudinal differences between the two continents and contributes to the latitudinal differences in gene expression. $\textbf{CONCLUSIONS}$: Both Australia and United States were relatively recently colonized by$\textit{ D. melanogaster}$, and it was recently shown that introductions of both African and European flies occurred, with African genotypes contributing disproportionately to tropical populations. Therefore, both the demographic history of the populations and local adaptation may be causing the patterns that we see.This work was funded by European Research Council grant DrosophilaInfection 281668 and the Natural Environment Research Council grant NE/L004232/1

Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares

Snowshoe hares (Lepus americanus) maintain seasonal camouflage by molting to a white winter coat, but some hares remain brown during the winter in regions with low snow cover. We show that cis-regulatory variation controlling seasonal expression of the Agouti gene underlies this adaptive winter camouflage polymorphism. Genetic variation at Agouti clustered by winter coat color across multiple hare and jackrabbit species, revealing a history of recurrent interspecific gene flow. Brown winter coats in snowshoe hares likely originated from an introgressed black-tailed jackrabbit allele that has swept to high frequency in mild winter environments. These discoveries show that introgression of genetic variants that underlie key ecological traits can seed past and ongoing adaptation to rapidly changing environments. (c) The Authors, Some Rights Reserved

Symbiont strain is the main determinant of variation in Wolbachia-mediated protection against viruses across Drosophila species

Wolbachia is a common heritable bacterial symbiont in insects. Its evolutionary success lies in the diverse phenotypic effects it has on its hosts coupled to its propensity to move between host species over evolutionary timescales. In a survey of natural host-symbiont associations in a range of Drosophila species, we found that 10 of 16 Wolbachia strains protected their hosts against viral infection. By moving Wolbachia strains between host species, we found that the symbiont genome had a much greater influence on the level of antiviral protection than the host genome. The reason for this was that the level of protection depended on the density of the symbiont in host tissues, and Wolbachia rather than the host-controlled density. The finding that virus resistance and symbiont density are largely under the control of symbiont genes in this system has important implications both for the evolution of these traits and for public health programmes using Wolbachia to prevent mosquitoes from transmitting disease.This study was funded by the Wellcome Trust grant WT094664MA (http://www.wellcome.ac.uk/) and the European Research Council (ERC) grant 281668 DrosophilaInfection

Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

In animals, small RNA molecules termed PIWI-interacting RNAs (piRNAs) silence transposable elements (TEs), protecting the germline from genomic instability and mutation. piRNAs have been detected in the soma in a few animals, but these are believed to be specific adaptations of individual species. Here, we report that somatic piRNAs were likely present in the ancestral arthropod more than 500 million years ago. Analysis of 20 species across the arthropod phylum suggests that somatic piRNAs targeting TEs and mRNAs are common among arthropods. The presence of an RNA-dependent RNA polymerase in chelicerates (horseshoe crabs, spiders, scorpions) suggests that arthropods originally used a plant-like RNA interference mechanism to silence TEs. Our results call into question the view that the ancestral role of the piRNA pathway was to protect the germline and demonstrate that small RNA silencing pathways have been repurposed for both somatic and germline functions throughout arthropod evolution.We thank A. McGregor, D. Leite, M. Akam, R. Jenner, R. Kilner, A. Duarte, C. Jiggins, R. Wallbank, A. Bourke, T. Dalmay, N. Moran, K. Warchol, R. Callahan, G. Farley and T. Livdahl for providing the arthropods. H. Robertson provided the D. virgifera genome sequence. This research was supported by a Leverhulme Research Project Grant (RPG-2016-210 to F.M.J., E.A.M. and P.S.), a European Research Council grant (281668 DrosophilaInfection to F.M.J.), a Medical Research Council grant (MRC MC-A652-5PZ80 to P.S.), an Imperial College Research Fellowship (to P.S.), Cancer Research UK (C13474/A18583 and C6946/A14492 to E.A.M.), the Wellcome Trust (104640/Z/14/Z and 092096/Z/10/Z to E.A.M.) and a National Institutes of Health R37 grant (GM62862 to P.D.Z.)

Quantifying Adaptive Evolution in the Drosophila Immune System

It is estimated that a large proportion of amino acid substitutions in Drosophila have been fixed by natural selection, and as organisms are faced with an ever-changing array of pathogens and parasites to which they must adapt, we have investigated the role of parasite-mediated selection as a likely cause. To quantify the effect, and to identify which genes and pathways are most likely to be involved in the host–parasite arms race, we have re-sequenced population samples of 136 immunity and 287 position-matched non-immunity genes in two species of Drosophila. Using these data, and a new extension of the McDonald-Kreitman approach, we estimate that natural selection fixes advantageous amino acid changes in immunity genes at nearly double the rate of other genes. We find the rate of adaptive evolution in immunity genes is also more variable than other genes, with a small subset of immune genes evolving under intense selection. These genes, which are likely to represent hotspots of host–parasite coevolution, tend to share similar functions or belong to the same pathways, such as the antiviral RNAi pathway and the IMD signalling pathway. These patterns appear to be general features of immune system evolution in both species, as rates of adaptive evolution are correlated between the D. melanogaster and D. simulans lineages. In summary, our data provide quantitative estimates of the elevated rate of adaptive evolution in immune system genes relative to the rest of the genome, and they suggest that adaptation to parasites is an important force driving molecular evolution

Comparisons of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity

Background Figs and fig-pollinating wasp species usually display a highly specific one-to-one association. However, more and more studies have revealed that the "one-to-one" rule has been broken. Co-pollinators have been reported, but we do not yet know how they evolve. They may evolve from insect speciation induced or facilitated by Wolbachia which can manipulate host reproduction and induce reproductive isolation. In addition, Wolbachia can affect host mitochondrial DNA evolution, because of the linkage between Wolbachia and associated mitochondrial haplotypes, and thus confound host phylogeny based on mtDNA. Previous research has shown that fig wasps have the highest incidence of Wolbachia infection in all insect taxa, and Wolbachia may have great influence on fig wasp biology. Therefore, we look forward to understanding the influence of Wolbachia on mitochondrial DNA evolution and speciation in fig wasps. Results We surveyed 76 pollinator wasp specimens from nine Ficus microcarpa trees each growing at a different location in Hainan and Fujian Provinces, China. We found that all wasps were morphologically identified as Eupristina verticillata, but diverged into three clades with 4.22-5.28% mtDNA divergence and 2.29-20.72% nuclear gene divergence. We also found very strong concordance between E. verticillata clades and Wolbachia infection status, and the predicted effects of Wolbachia on both mtDNA diversity and evolution by decreasing mitochondrial haplotypes. Conclusions Our study reveals that the pollinating wasp E. verticillata on F. microcarpa has diverged into three cryptic species, and Wolbachia may have a role in this divergence. The results also indicate that Wolbachia strains infecting E. verticillata have likely resulted in selective sweeps on host mitochondrial DNA

The evolution of transmission mode

This article reviews research on the evolutionary mechanisms leading to different transmission modes. Such modes are often under genetic control of the host or the pathogen, and often in conflict with each other via trade-offs. Transmission modes may vary among pathogen strains and among host populations. Evolutionary changes in transmission mode have been inferred through experimental and phylogenetic studies, including changes in transmission associated with host-shifts and with evolution of the unusually complex life cycles of many parasites. Understanding the forces that determine the evolution of particular transmission modes presents a fascinating medley of problems for which there is a lack of good data and often a lack of conceptual understanding or appropriate methodologies. Our best information comes from studies that have been focused on the vertical vs. horizontal transmission dichotomy. With other kinds of transitions, theoretical approaches combining epidemiology and population genetics are providing guidelines for determining when and how rapidly new transmission modes may evolve, but these are still in need of empirical investigation and application to particular cases. Obtaining such knowledge is a matter of urgency in relation to extant disease threats

Wolbachia and DNA barcoding insects: patterns, potential and problems

Wolbachia is a genus of bacterial endosymbionts that impacts the breeding systems of their hosts. Wolbachia can confuse the patterns of mitochondrial variation, including DNA barcodes, because it influences the pathways through which mitochondria are inherited. We examined the extent to which these endosymbionts are detected in routine DNA barcoding, assessed their impact upon the insect sequence divergence and identification accuracy, and considered the variation present in Wolbachia COI. Using both standard PCR assays (Wolbachia surface coding protein – wsp), and bacterial COI fragments we found evidence of Wolbachia in insect total genomic extracts created for DNA barcoding library construction. When >2 million insect COI trace files were examined on the Barcode of Life Datasystem (BOLD) Wolbachia COI was present in 0.16% of the cases. It is possible to generate Wolbachia COI using standard insect primers; however, that amplicon was never confused with the COI of the host. Wolbachia alleles recovered were predominantly Supergroup A and were broadly distributed geographically and phylogenetically. We conclude that the presence of the Wolbachia DNA in total genomic extracts made from insects is unlikely to compromise the accuracy of the DNA barcode library; in fact, the ability to query this DNA library (the database and the extracts) for endosymbionts is one of the ancillary benefits of such a large scale endeavor – for which we provide several examples. It is our conclusion that regular assays for Wolbachia presence and type can, and should, be adopted by large scale insect barcoding initiatives. While COI is one of the five multi-locus sequence typing (MLST) genes used for categorizing Wolbachia, there is limited overlap with the eukaryotic DNA barcode region