Recent and Recurrent Selective Sweeps of the Antiviral RNAi Gene Argonaute-2 in Three Species of Drosophila

Antagonistic host–parasite interactions can drive rapid adaptive evolution in genes of the immune system, and such arms races may be an important force shaping polymorphism in the genome. The RNA interference pathway gene Argonaute-2 (AGO2) is a key component of antiviral defense in Drosophila, and we have previously shown that genes in this pathway experience unusually high rates of adaptive substitution. Here we study patterns of genetic variation in a 100-kbp region around AGO2 in three different species of Drosophila. Our data suggest that recent independent selective sweeps in AGO2 have reduced genetic variation across a region of more than 50 kbp in Drosophila melanogaster, D. simulans, and D. yakuba, and we estimate that selection has fixed adaptive substitutions in this gene every 30–100 thousand years. The strongest signal of recent selection is evident in D. simulans, where we estimate that the most recent selective sweep involved an allele with a selective advantage of the order of 0.5–1% and occurred roughly 13–60 Kya. To evaluate the potential consequences of the recent substitutions on the structure and function of AGO2, we used fold-recognition and homology-based modeling to derive a structural model for the Drosophila protein, and this suggests that recent substitutions in D. simulans are overrepresented at the protein surface. In summary, our results show that selection by parasites can consistently target the same genes in multiple species, resulting in areas of the genome that have markedly reduced genetic diversity

Phenotypic plasticity of nest timing in a post‐glacial landscape: how do reptiles adapt to seasonal time constraints?

Life histories evolve in response to constraints on the time available for growth and development. Nesting date and its plasticity in response to spring temperature may therefore be important components of fitness in oviparous ectotherms near their northern range limit, as reproducing early provides more time for embryos to complete development before winter. We used data collected over several decades to compare air temperature and nest date plasticity in populations of painted turtles and snapping turtles from a relatively warm environment (southeastern Michigan) near the southern extent of the last glacial maximum to a relatively cool environment (central Ontario) near the northern extent of post‐glacial recolonization. For painted turtles, population‐level differences in reaction norm elevation for two phenological traits were consistent with adaptation to time constraints, but no differences in reaction norm slopes were observed. For snapping turtle populations, the difference in reaction norm elevation for a single phenological trait was in the opposite direction of what was expected under adaptation to time constraints, and no difference in reaction norm slope was observed. Finally, among‐individual variation in individual plasticity for nesting date was detected only in the northern population of snapping turtles, suggesting that reaction norms are less canalized in this northern population. Overall, we observed evidence of phenological adaptation, and possibly maladaptation, to time constraints in long‐lived reptiles. Where present, (mal)adaptation occurred by virtue of differences in reaction norm elevation, not reaction norm slope. Glacial history, generation time, and genetic constraint may all play an important role in the evolution of phenological timing and its plasticity in long‐lived reptiles

Population-genomic analysis identifies a low rate of global adaptive fixation in the proteins of the cyclical parthenogen Daphnia magna

Daphnia are well-established ecological and evolutionary models, and the interaction between D. magna and its microparasites is widely considered a paragon of the host-parasite coevolutionary process. Like other well-studied arthropods such as Drosophila melanogaster and Anopheles gambiae, D. magna is a small, widespread, and abundant species that is therefore expected to display a large long-term population size and high rates of adaptive protein evolution. However, unlike these other species, D. magna is cyclically asexual and lives in a highly structured environment (ponds and lakes) with moderate levels of dispersal, both of which are predicted to impact upon long-term effective population size and adaptive protein evolution. To investigate patterns of adaptive protein fixation, we produced the complete coding genomes of 36 D. magna clones sampled from across the European range (Western Palaearctic), along with draft sequences for the close relatives D. similis and D. lumholtzi, used as outgroups. We analyzed genome-wide patterns of adaptive fixation, with a particular focus on genes that have an a priori expectation of high rates, such as those likely to mediate immune responses, RNA interference against viruses and transposable elements, and those with a strongly male-biased expression pattern. We find that, as expected, D. magna displays high levels of diversity and that this is highly structured among populations. However, compared to Drosophila, we find that D. magna proteins appear to have a high proportion of weakly deleterious variants and do not show evidence of pervasive adaptive fixation across its entire range. This is true of the genome as a whole, and also of putative ‘arms race’ genes that often show elevated levels of adaptive substitution in other species. In addition to the likely impact of extensive, and previously documented, local adaptation, we speculate that these findings may reflect reduced efficacy of selection associated with cyclical asexual reproduction

Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny

The sigma virus (DMelSV), which is a natural pathogen of Drosophila melanogaster, is the only Drosophila-specific rhabdovirus that has been described. We have discovered two new rhabdoviruses, D. obscura and D. affinis, which we have named DObsSV and DAffSV, respectively. We sequenced the complete genomes of DObsSV and DMelSV, and the L gene from DAffSV. Combining these data with sequences from a wide range of other rhabdoviruses, we found that the three sigma viruses form a distinct clade which is a sister group to the Dimarhabdovirus supergroup, and the high levels of divergence between these viruses suggest that they deserve to be recognized as a new genus. Furthermore, our analysis produced the most robustly supported phylogeny of the Rhabdoviridae to date, allowing us to reconstruct the major transitions that have occurred during the evolution of the family. Our data suggest 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

Host-switching by a vertically transmitted rhabdovirus in Drosophila

A diverse range of endosymbionts are found within the cells of animals. As these endosymbionts are normally vertically transmitted, we might expect their evolutionary history to be dominated by host-fidelity and cospeciation with the host. However, studies of bacterial endosymbionts have shown that while this is true for some mutualists, parasites often move horizontally between host lineages over evolutionary timescales. For the first time, to our knowledge, we have investigated whether this is also the case for vertically transmitted viruses. Here, we describe four new sigma viruses, a group of vertically transmitted rhabdoviruses previously known in Drosophila. Using sequence data from these new viruses, and the previously described sigma viruses, we show that they have switched between hosts during their evolutionary history. Our 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

Exceptional Diversity, Maintenance of Polymorphism, and Recent Directional Selection on the APL1 Malaria Resistance Genes of Anopheles gambiae

The three-gene APL1 locus encodes essential components of the mosquito immune defense against malaria parasites. APL1 was originally identified because it lies within a mapped QTL conferring the vector mosquito Anopheles gambiae natural resistance to the human malaria parasite, Plasmodium falciparum, and APL1 genes have subsequently been shown to be involved in defense against several species of Plasmodium. Here, we examine molecular population genetic variation at the APL1 gene cluster in spatially and temporally diverse West African collections of A. gambiae. The locus is extremely polymorphic, showing evidence of adaptive evolutionary maintenance of genetic variation. We hypothesize that this variability aids in defense against genetically diverse pathogens, including Plasmodium. Variation at APL1 is highly structured across geographic and temporal subpopulations. In particular, diversity is exceptionally high during the rainy season, when malaria transmission rates are at their peak. Much less allelic diversity is observed during the dry season when mosquito population sizes and malaria transmission rates are low. APL1 diversity is weakly stratified by the polymorphic 2La chromosomal inversion but is very strongly subdivided between the M and S “molecular forms.” We find evidence that a recent selective sweep has occurred at the APL1 locus in M form mosquitoes only. The independently reported observation of a similar M-form restricted sweep at the Tep1 locus, whose product physically interacts with APL1C, suggests that epistatic selection may act on these two loci causing them to sweep coordinately

Adaptive Evolution of a Stress Response Protein

Some cancers are mediated by an interplay between tissue damage, pathogens and localised innate immune responses, but the mechanisms that underlie these linkages are only beginning to be unravelled.Here we identify a strong signature of adaptive evolution on the DNA sequence of the mammalian stress response gene SEP53, a member of the epidermal differentiation complex fused-gene family known for its role in suppressing cancers. The SEP53 gene appears to have been subject to adaptive evolution of a type that is commonly (though not exclusively) associated with coevolutionary arms races. A similar pattern of molecular evolution was not evident in the p53 cancer-suppressing gene.Our data thus raises the possibility that SEP53 is a component of the mucosal/epithelial innate immune response engaged in an ongoing interaction with a pathogen. Although the pathogenic stress mediating adaptive evolution of SEP53 is not known, there are a number of well-known candidates, in particular viruses with established links to carcinoma

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

Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts

Pathogens switching to new hosts can result in the emergence of new infectious diseases, and determining which species are likely to be sources of such host shifts is essential to understanding disease threats to both humans and wildlife. However, the factors that determine whether a pathogen can infect a novel host are poorly understood. We have examined the ability of three host-specific RNA-viruses (Drosophila sigma viruses from the family Rhabdoviridae) to persist and replicate in 51 different species of Drosophilidae. Using a novel analytical approach we found that the host phylogeny could explain most of the variation in viral replication and persistence between different host species. This effect is partly driven by viruses reaching a higher titre in those novel hosts most closely related to the original host. However, there is also a strong effect of host phylogeny that is independent of the distance from the original host, with viral titres being similar in groups of related hosts. Most of this effect could be explained by variation in general susceptibility to all three sigma viruses, as there is a strong phylogenetic correlation in the titres of the three viruses. These results suggest that the source of new emerging diseases may often be predictable from the host phylogeny, but that the effect may be more complex than simply causing most host shifts to occur between closely related hosts