Host adaptation to viruses relies on few genes with different cross-resistance properties

Martins, Nelson; Faria, Vítor G.; Nolte, Viola; Schlötterer, Christian; Teixeira, Luı́s; Sucena, Élio; Magalhães, Sara

doi:10.1073/pnas.1400378111

Cited by 121 publications

(220 citation statements)

References 49 publications

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“…2011, 2012; Martins et al . 2014). The other group of natural parasites that is well‐studied in D. melanogaster is parasitoid wasps, and here, a few major‐effect loci control resistance (Poirie et al .…”

Section: Discussionmentioning

confidence: 99%

The genetic architecture of resistance to virus infection in Drosophila

et al. 2016

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Variation in susceptibility to infection has a substantial genetic component in natural populations, and it has been argued that selection by pathogens may result in it having a simpler genetic architecture than many other quantitative traits. This is important as models of host–pathogen co‐evolution typically assume resistance is controlled by a small number of genes. Using the Drosophila melanogaster multiparent advanced intercross, we investigated the genetic architecture of resistance to two naturally occurring viruses, the sigma virus and DCV (Drosophila C virus). We found extensive genetic variation in resistance to both viruses. For DCV resistance, this variation is largely caused by two major‐effect loci. Sigma virus resistance involves more genes – we mapped five loci, and together these explained less than half the genetic variance. Nonetheless, several of these had a large effect on resistance. Models of co‐evolution typically assume strong epistatic interactions between polymorphisms controlling resistance, but we were only able to detect one locus that altered the effect of the main effect loci we had mapped. Most of the loci we mapped were probably at an intermediate frequency in natural populations. Overall, our results are consistent with major‐effect genes commonly affecting susceptibility to infectious diseases, with DCV resistance being a near‐Mendelian trait.

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Section: Discussionmentioning

confidence: 99%

The genetic architecture of resistance to virus infection in Drosophila

et al. 2016

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“…It could be expected that tradeoffs in the adaptation to distantly related plants would enable speciation via host shift (17). However, recent experimental studies question the existence of such tradeoffs in the evolution of both parasites (38) and hosts (44). In fact, the evolution of new parasite species by host shifts has been found to be overestimated (13) or predominantly allopatric (20).…”

Section: Discussionmentioning

confidence: 99%

Geography and major host evolutionary transitions shape the resource use of plant parasites

Calatayud

Hórreo

Madrigal‐González

et al. 2016

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

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The evolution of resource use in herbivores has been conceptualized as an analog of the theory of island biogeography, assuming that plant species are islands separated by phylogenetic distances. Despite its usefulness, this analogy has paradoxically led to neglecting real biogeographical processes in the study of macroevolutionary patterns of herbivore-plant interactions. Here we show that host use is mostly determined by the geographical cooccurrence of hosts and parasites in spider mites (Tetranychidae), a globally distributed group of plant parasites. Strikingly, geography accounts for most of the phylogenetic signal in host use by these parasites. Beyond geography, only evolutionary transitions among major plant lineages (i.e., gymnosperms, commelinids, and eudicots) shape resource use patterns in these herbivores. Still, even these barriers have been repeatedly overcome in evolutionary time, resulting in phylogenetically diverse parasite communities feeding on similar hosts. Therefore, our results imply that patterns of apparent evolutionary conservatism may largely be a byproduct of the geographic cooccurrence of hosts and parasites.evolutionary conservatism | geographic signal | host use evolution | parasite-host interactions | spider mites E cological interactions are commonly thought to be evolutionarily conserved (1). This idea roots back to Darwin and is based on the assumption that traits regulating interactions are mainly an ancestor's legacy. Following this rationale, it is expected that phylogenetically related species will also interact with partners that are phylogenetically clustered. Plants and the herbivores that feed on them constitute a large amount of the Earth's terrestrial biodiversity. However, the processes behind the origin of such diversity remain controversial (2). Related plant hosts tend to harbor similar communities of both herbivores (3-5) and pathogens (6, 7). Still, host shifts may be favored when they involve distantly related plants producing similar chemical compounds as defense against parasites (8). In fact, macroevolutionary evidence shows that host shifts of parasites to unrelated plants are common (9-13), questioning the ubiquity of evolutionary conservatism.These patterns of host use in parasites have led to the formulation of the "parasite paradox," which states that although parasites are generally specialized on a given (set of) host plant(s), host shifts to distantly related hosts occur frequently (14, 15). Further, the frequent shifts between evolutionarily distinct hosts observed in parasites have led to the analogy of considering plant species as resource islands separated by evolutionary distances (16)(17)(18). In this metaphor, related plants constitute resource archipelagos within which colonization of new resource islands entails few costs. Among such archipelagos, however, colonization processes may be costly, potentially leading to disruptive selection and hence to speciation via host shift (19,20). Paradoxically, framing the evolution of plant host use ...

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“…Previous studies have revealed that insect susceptibility to viral infection is determined by host factors, which either facilitate (6,7) or restrict viral replication (8)(9)(10). In addition, the bacterial flora, particularly endosymbiotic Wolbachia strains, modifies susceptibility to viral infections (11,12).…”

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confidence: 99%

Cytokine Diedel and a viral homologue suppress the IMD pathway in Drosophila

Lamiable

Kellenberger

Kemp

et al. 2016

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

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Viruses are obligatory intracellular parasites that suffer strong evolutionary pressure from the host immune system. Rapidly evolving viral genomes can adapt to this pressure by acquiring genes that counteract host defense mechanisms. For example, many vertebrate DNA viruses have hijacked cellular genes encoding cytokines or cytokine receptors to disrupt host cell communication. Insect viruses express suppressors of RNA interference or apoptosis, highlighting the importance of these cell intrinsic antiviral mechanisms in invertebrates. Here, we report the identification and characterization of a family of proteins encoded by insect DNA viruses that are homologous to a 12-kDa circulating protein encoded by the virus-induced Drosophila gene diedel (die). We show that die mutant flies have shortened lifespan and succumb more rapidly than controls when infected with Sindbis virus. This reduced viability is associated with deregulated activation of the immune deficiency (IMD) pathway of host defense and can be rescued by mutations in the genes encoding the homolog of IKKγ or IMD itself. Our results reveal an endogenous pathway that is exploited by insect viruses to modulate NF-κB signaling and promote fly survival during the antiviral response.

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Host adaptation to viruses relies on few genes with different cross-resistance properties

Cited by 121 publications

References 49 publications

The genetic architecture of resistance to virus infection in Drosophila

The genetic architecture of resistance to virus infection in Drosophila

Geography and major host evolutionary transitions shape the resource use of plant parasites

Cytokine Diedel and a viral homologue suppress the IMD pathway in Drosophila

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