Influence of the Virus LbFV and of Wolbachia in a Host-Parasitoid Interaction

Martinez, Julien; Duplouy, Anne; Woolfit, Megan; Vavre, Fabrice; O'Neill, Scott Leslie; Varaldi, Julien

doi:10.1371/journal.pone.0035081

Cited by 32 publications

(29 citation statements)

References 58 publications

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“…Lack of a significant effect of wMel on the interaction of Lb with D. melanogaster (two backgrounds) was also reported by Martinez et al (2012). Other strains of Wolbachia are reported to have negative and positive effects on the interaction of D. simulans with Lb (Fytrou et al, 2006;Martinez et al, 2012), but these effects are dependent on whether or not Lb carries the virus LbFV (Martinez et al, 2012), which does not occur in the Lb strain used in our study (Gueguen et al, 2011). Thus, it appears that in D. melanogaster, at least, Wolbachia wMel does not significantly influence the outcome of oviposition by Lb.…”

Section: Discussionsupporting

confidence: 57%

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

et al. 2013

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Maternally transmitted associations between endosymbiotic bacteria and insects are diverse and widespread in nature. Owing to imperfect vertical transmission, many heritable microbes have evolved compensational mechanisms to enhance their persistence in host lineages, such as manipulating host reproduction and conferring fitness benefits to host. Symbiont-mediated defense against natural enemies of hosts is increasingly recognized as an important mechanism by which endosymbionts enhance host fitness. Members of the genus Spiroplasma associated with distantly related Drosophila hosts are known to engage in either reproductive parasitism (i.e., male killing) or defense against natural enemies (the parasitic wasp Leptopilina heterotoma and a nematode). A male-killing strain of Spiroplasma (strain Melanogaster Sex Ratio Organism (MSRO)) co-occurs with Wolbachia (strain wMel) in certain wild populations of the model organism Drosophila melanogaster. We examined the effects of Spiroplasma MSRO and Wolbachia wMel on Drosophila survival against parasitism by two common wasps, Leptopilina heterotoma and Leptopilina boulardi, that differ in their host ranges and host evasion strategies. The results indicate that Spiroplasma MSRO prevents successful development of both wasps, and confers a small, albeit significant, increase in larva-toadult survival of flies subjected to wasp attacks. We modeled the conditions under which defense can contribute to Spiroplasma persistence. Wolbachia also confers a weak, but significant, survival advantage to flies attacked by L. heterotoma. The host protective effects exhibited by Spiroplasma and Wolbachia are additive and may provide the conditions for such cotransmitted symbionts to become mutualists. Occurrence of Spiroplasma-mediated protection against distinct parasitoids in divergent Drosophila hosts suggests a general protection mechanism.

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Section: Discussionsupporting

confidence: 57%

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

et al. 2013

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“…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. Thus, the role of Wolbachia in the susceptibility to other parasites appears extremely variable between host-Wolbachia-parasite systems, and may depend on the Wolbachia strain and the host genotype or species (Bordenstein et al, 2003;Hornett et al, 2008).…”

Section: Introductionmentioning

confidence: 94%

“…These studies are mostly laboratory based, with just a few using natural host populations (Skelton et al, 2016;Zele et al, 2014), and only some with parasitoids rather than pathogen infection (Fytrou et al, 2006;Hsiao, 1996;Martinez et al, 2012;Xie et al, 2014). In order to understand the complex role of endosymbionts, such studies should also be conducted under natural conditions, and in a broad range of host taxa.…”

Section: Introductionmentioning

confidence: 99%

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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“…For instance, females have similar lifetime expectancy, although they incur a modest cost on size (Varaldi et al 2005). Interestingly, the virus also brings a slight protection for the wasp egg against the immune reaction of some Drosophila strains (Martinez et al 2012), underlying the multidimensionalty of the relationship between the virus and the wasp.…”

Section: Introductionmentioning

confidence: 99%

Genome Sequencing of the Behavior Manipulating Virus LbFV Reveals a Possible New Virus Family

Lepetit

Gillet

Hughes

et al. 2016

Genome Biology and Evolution

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Parasites are sometimes able to manipulate the behavior of their hosts. However, the molecular cues underlying this phenomenon are poorly documented. We previously reported that the parasitoid wasp Leptopilina boulardi which develops from Drosophila larvae is often infected by an inherited DNA virus. In addition to being maternally transmitted, the virus benefits from horizontal transmission in superparasitized larvae (Drosophila that have been parasitized several times). Interestingly, the virus forces infected females to lay eggs in already parasitized larvae, thus increasing the chance of being horizontally transmitted. In a first step towards the identification of virus genes responsible for the behavioral manipulation, we present here the genome sequence of the virus, called LbFV. The sequencing revealed that its genome contains an homologous repeat sequence (hrs) found in eight regions in the genome. The presence of this hrs may explain the genomic plasticity that we observed for this genome. The genome of LbFV encodes 108 ORFs, most of them having no homologs in public databases. The virus is however related to Hytrosaviridae, although distantly. LbFV may thus represent a member of a new virus family. Several genes of LbFV were captured from eukaryotes, including two anti-apoptotic genes. More surprisingly, we found that LbFV captured from an ancestral wasp a protein with a Jumonji domain. This gene was afterwards duplicated in the virus genome. We hypothesized that this gene may be involved in manipulating the expression of wasp genes, and possibly in manipulating its behavior.

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Influence of the Virus LbFV and of Wolbachia in a Host-Parasitoid Interaction

Cited by 32 publications

References 58 publications

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

Wolbachiaincreases the susceptibility of a parasitoid wasp to hyperparasitism

Genome Sequencing of the Behavior Manipulating Virus LbFV Reveals a Possible New Virus Family

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