Symbionts Commonly Provide Broad Spectrum Resistance to Viruses in Insects: A Comparative Analysis of Wolbachia Strains

Martinez, Julien; Longdon, Ben; Bauer, Simone; Chan, Yuk-Sang; Miller, Wolfgang J.; Bourtzis, Kostas; Teixeira, Luı́s; Jiggins, Francis M.

doi:10.1371/journal.ppat.1004369

Cited by 237 publications

(292 citation statements)

References 97 publications

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“…10% of the lines were tested by standard qPCR (Martinez et al . 2014), and none were infected. We used PCR to genotype the founder lines and selected RILs for polymorphisms in the genes ref(2)p and CHKov1 that have been previously associated with virus resistance.…”

Section: Methodsmentioning

confidence: 96%

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: Methodsmentioning

confidence: 96%

The genetic architecture of resistance to virus infection in Drosophila

et al. 2016

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“…Thus, the Wolbachia strains present in higher density in D. melanogaster also shorten the flies' lifespan (Chrostek et al, 2013(Chrostek et al, , 2014. Therefore, if the selection pressure from parasites is weak, there is little chance that the Wolbachia strain would spread in its host population (Martinez et al, 2014(Martinez et al, , 2015. Hence, the presence of Wolbachia is not always only beneficial with respect to immunity (Table 1).…”

Section: Statistical Modelsmentioning

confidence: 99%

“…Wolbachia induce upregulation of several host immune genes (Bian et al, 2010;Hughes et al, 2011;Kambris et al, 2010Kambris et al, , 2009, potentially priming the immune system to respond strongly to pathogens or parasitoids (but see Bourtzis et al, 2000). Alternatively, Wolbachia may reduce the fitness of invading pathogens by competing for resources (Martinez et al, 2014;Moreira et al, 2009;Osborne et al, 2009). As we found no evidence of encapsulation of M. cf.…”

Section: Statistical Modelsmentioning

confidence: 99%

“…The ability to improve host resistance is, however, not pervasive across all host-Wolbachia-parasite interactions. Thus, the presence of Wolbachia in D. simulans did not always improve the flies' resistance to the fungal pathogen Beauveria bassiana (Fytrou et al, 2006), diverse viruses (Martinez et al, 2014;Osborne et al, 2009) or bacteria (Wong et al, 2011). Furthermore, although Martinez et al (2012) found no effect of wRi in flies parasitized by the parasitoid wasp Leptopilina boulardi, Fytrou et al (2006) showed that the same endosymbiotic bacterial strain increased the susceptibility of the flies to the closely related parasitoid wasp L. heterotoma.…”

Section: Introductionmentioning

confidence: 99%

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Wolbachiaincreases the susceptibility of a parasitoid wasp to hyperparasitism

Nouhuys

Kohonen

Duplouy

2016

Journal of Experimental Biology

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The success of maternally transmitted endosymbiotic bacteria, such as Wolbachia, is directly linked to their host reproduction but in direct conflict with other parasites that kill the host before it reaches reproductive maturity. Therefore, symbionts that have evolved strategies to increase their host’s ability to evade lethal parasites may have high penetrance, while detrimental symbionts would be selected against, leading to lower penetrance or extinction from the host population. In a natural population of the parasitoid wasp Hyposoter horticola in the Åland Islands (Finland), the Wolbachia strain wHho persists at an intermediate prevalence (∼50%). Additionally, there is a negative correlation between the prevalence of Wolbachia and a hyperparasitoid wasp, Mesochorus cf. stigmaticus, in the landscape. Using a manipulative field experiment, we addressed the persistence of Wolbachia at this intermediate level, and tested whether the observed negative correlation could be due to Wolbachia inducing either susceptibility or resistance to parasitism. We show that infection with Wolbachia does not influence the ability of the wasp to parasitize its butterfly host, Melitaea cinxia, but that hyperparasitism of the wasp increases in the presence of wHho. Consequently, the symbiont is detrimental, and in order to persist in the host population, must also have a positive effect on fitness that outweighs the costly burden of susceptibility to widespread parasitism.

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“…The Drosophila-Wolbachia pairings CO-wAu, DSR-wRi, w1118-wMel, and the overreplicating and life-shortening w1118-wMelPop association all show a delay in DCV-induced mortality when DCV is injected into adult flies, while the N7NO-wNo and DSH-wHa combinations did not (2,3,11, 29). A feature that all protective Wolbachia strains share is high density within their respective host organism, indicating that high Wolbachia density may serve as a prerequisite for antiviral protection (7,12,(29)(30)(31)(32)(33)(34).Wolbachia is estimated to infect 40% of all insects (35); therefore, the effect it exerts on natural viral dynamics could be pronounced. The understanding of natural tripartite Drosophila-virus-Wolbachia interactions is very limited at present, partially due to a lack of a method for orally delivering the virus.…”

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confidence: 99%

Wolbachia-Mediated Antiviral Protection in Drosophila Larvae and Adults following Oral Infection

Stevanovic

Arnold

Johnson

2015

Appl Environ Microbiol

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Understanding viral dynamics in arthropods is of great importance when designing models to describe how viral spread can influence arthropod populations. The endosymbiotic bacterium Wolbachia spp., which is present in up to 40% of all insect species, has the ability to alter viral dynamics in both Drosophila spp. and mosquitoes, a feature that in mosquitoes may be utilized to limit spread of important arboviruses. To understand the potential effect of Wolbachia on viral dynamics in nature, it is important to consider the impact of natural routes of virus infection on Wolbachia antiviral effects. Using adult Drosophila strains, we show here that Drosophila-Wolbachia associations that have previously been shown to confer antiviral protection following systemic viral infection also confer protection against virus-induced mortality following oral exposure to Drosophila C virus in adults. Interestingly, a different pattern was observed when the same fly lines were challenged with the virus when still larvae. Analysis of the four Drosophila-Wolbachia associations that were protective in adults indicated that only the w1118-wMelPop association conferred protection in larvae following oral delivery of the virus. Analysis of Wolbachia density using quantitative PCR (qPCR) showed that a high Wolbachia density was congruent with antiviral protection in both adults and larvae. This study indicates that Wolbachia-mediated protection may vary between larval and adult stages of a given Wolbachia-host combination and that the variations in susceptibility by life stage correspond with Wolbachia density. The differences in the outcome of virus infection are likely to influence viral dynamics in Wolbachia-infected insect populations in nature and could also have important implications for the transmission of arboviruses in mosquito populations.A rthropods harbor a wide range of viruses that can be transmitted between individuals or populations of the same species or can bridge the interspecies gap to infect plants or other animals. The outcome of viral infections can be modulated by tripartite interactions between arthropods, viruses, and bacteria (1). One such interaction is the tripartite interaction between insects, viruses, and the endosymbyotic bacterium Wolbachia pipientis.Wolbachia spp. have gained much attention due to the antiviral effects they confer to their host. The impact of Wolbachia spp. on virus infection was first described in the Drosophila melanogaster host, where it was shown to protect against mortality induced by diverse viruses, including Drosophila C virus (DCV), cricket paralysis virus, and Flock House virus (2, 3). Since that discovery, Wolbachia-mediated antiviral effects have been demonstrated in a number of insect hosts and are being investigated as a way of limiting spread of arboviruses (reviewed in references 1, 4, 5, and 6). Notably, Wolbachia-mediated antiviral effects have been demonstrated in adult mosquitoes artificially infected with Wolbachia; in mosquitoes, Wolbachia can interfere with accu...

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Symbionts Commonly Provide Broad Spectrum Resistance to Viruses in Insects: A Comparative Analysis of Wolbachia Strains

Cited by 237 publications

References 97 publications

The genetic architecture of resistance to virus infection in Drosophila

The genetic architecture of resistance to virus infection in Drosophila

Wolbachiaincreases the susceptibility of a parasitoid wasp to hyperparasitism

Wolbachia-Mediated Antiviral Protection in Drosophila Larvae and Adults following Oral Infection

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