Recurrent Adaptation in RNA Interference Genes Across the Drosophila Phylogeny

Kolaczkowski, Bryan; Hupalo, Daniel; Kern, Andrew D.

doi:10.1093/molbev/msq284

Cited by 79 publications

(100 citation statements)

References 64 publications

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“…Contrary to this, genes involved in humoral defense and phagocytosis had low proportions of adaptive substitutions relative to the control set ( Figure 2A). The estimated a for viral response genes was not elevated, a result that may appear surprising given that viral response genes, and in particular genes involved in RNAi, are among the fastest evolving genes across the Drosophila phylogeny (Obbard et al 2006(Obbard et al , 2009Kolaczkowski et al 2011a). These genes, however, did have a markedly higher rate of adaptive substitution (v a ) relative to control estimates ( Figure 2B).…”

Section: Patterns Of D Melanogaster-d Simulans Divergence Differ Ammentioning

confidence: 87%

Survey of Global Genetic Diversity Within theDrosophilaImmune System

et al. 2017

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Numerous studies across a wide range of taxa have demonstrated that immune genes are routinely among the most rapidly evolving genes in the genome. This observation, however, does not address what proportion of immune genes undergo strong selection during adaptation to novel environments. Here, we determine the extent of very recent divergence in genes with immune function across five populations of Drosophila melanogaster and find that immune genes do not show an overall trend of recent rapid adaptation. Our population-based approach uses a set of carefully matched control genes to account for the effects of demography and local recombination rate, allowing us to identify whether specific immune functions are putative targets of strong selection. We find evidence that viral-defense genes are rapidly evolving in Drosophila at multiple timescales. Local adaptation to bacteria and fungi is less extreme and primarily occurs through changes in recognition and effector genes rather than large-scale changes to the regulation of the immune response. Surprisingly, genes in the Toll pathway, which show a high rate of adaptive substitution between the D. melanogaster and D. simulans lineages, show little population differentiation. Quantifying the flies for resistance to a generalist Gram-positive bacterial pathogen, we found that this genetic pattern of low population differentiation was recapitulated at the phenotypic level. In sum, our results highlight the complexity of immune evolution and suggest that Drosophila immune genes do not follow a uniform trajectory of strong directional selection as flies encounter new environments.

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Section: Patterns Of D Melanogaster-d Simulans Divergence Differ Ammentioning

confidence: 87%

Survey of Global Genetic Diversity Within theDrosophilaImmune System

et al. 2017

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“…Ago-2 is a clear example of this observation (55). Interestingly, genes in the piRNA pathway, including Piwi and Aub, also evolve very rapidly, which has been suggested to be caused by adaptation to the ever-changing landscape of transposition activity in the fly (55,56). The possibility that through regulation of transposons in somatic and germ-line tissues, the piRNA pathway could tune or control in a subtle manner the immune state of the host by genes involved in immunity cannot be disregarded.…”

Section: Discussionmentioning

confidence: 98%

piRNA pathway is not required for antiviral defense in Drosophila melanogaster

Petit

Mongelli

Frangeul

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Since its discovery, RNA interference has been identified as involved in many different cellular processes, and as a natural antiviral response in plants, nematodes, and insects. In insects, the small interfering RNA (siRNA) pathway is the major antiviral response. In recent years, the Piwi-interacting RNA (piRNA) pathway also has been implicated in antiviral defense in mosquitoes infected with arboviruses. Using Drosophila melanogaster and an array of viruses that infect the fruit fly acutely or persistently or are vertically transmitted through the germ line, we investigated in detail the extent to which the piRNA pathway contributes to antiviral defense in adult flies. Following virus infection, the survival and viral titers of Piwi, Aubergine, Argonaute-3, and Zucchini mutant flies were similar to those of wild type flies. Using next-generation sequencing of small RNAs from wild type and siRNA mutant flies, we showed that no viral-derived piRNAs were produced in fruit flies during different types of viral infection. Our study provides the first evidence, to our knowledge, that the piRNA pathway does not play a major role in antiviral defense in adult Drosophila and demonstrates that viral-derived piRNA production depends on the biology of the host–virus combination rather than being part of a general antiviral process in insects.

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“…Only 16 out of 23 RNAi genes studied by Obbard et al (2006Obbard et al ( , 2009a and Kolaczkowski et al (2011) were included in the initial D. mauritiana annotation. Hence, we manually curated the annotation of the seven missing RNAi genes (AGO2, armi, krimp, AGO3, mael, rhi, and squ).…”

Section: Signatures Of Positive Selection In D Mauritianamentioning

confidence: 99%

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

Nolte¹,

Pandey²,

Kofler³

et al. 2012

Genome Res.

117

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Although it is well understood that selection shapes the polymorphism pattern in Drosophila, signatures of classic selective sweeps are scarce. Here, we focus on Drosophila mauritiana, an island endemic, which is closely related to Drosophila melanogaster. Based on a new, annotated genome sequence, we characterized the genome-wide polymorphism by sequencing pooled individuals (Pool-seq). We show that the interplay between selection and recombination results in a genome-wide polymorphism pattern characteristic for D. mauritiana. Two large genomic regions (>500 kb) showed the signature of almost complete selective sweeps. We propose that the absence of population structure and limited geographic distribution could explain why such pronounced sweep patterns are restricted to D. mauritiana. Further evidence for strong adaptive evolution was detected for several nucleoporin genes, some of which were not previously identified as genes involved in genomic conflict. Since this adaptive evolution is continuing after the split of D. mauritiana and Drosophila simulans, we conclude that genomic conflict is not restricted to short episodes, but rather an ongoing process in Drosophila.

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Recurrent Adaptation in RNA Interference Genes Across the Drosophila Phylogeny

Cited by 79 publications

References 64 publications

Survey of Global Genetic Diversity Within theDrosophilaImmune System

Survey of Global Genetic Diversity Within theDrosophilaImmune System

piRNA pathway is not required for antiviral defense in Drosophila melanogaster

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

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