Unrelated facultative endosymbionts protect aphids against a fungal pathogen

Łukasik, Piotr; Asch, Margriet van; Guo, Huifang; Ferrari, Julia; Godfray, H. Charles J.

doi:10.1111/ele.12031

Cited by 276 publications

(252 citation statements)

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“…In all three of these cases (X, H, and XH) reductions in sporulation were small relative to that observed for aphids infected with R. insecticola (Fig. 4) 29.55 and P Յ 0.0001 [24,39]). HFS-infected lines also showed increased host mortality after pathogen exposure, which may be responsible for the observed reduction in sporulation ( No clear indication of antagonistic interactions between superinfecting HFS based on estimates of within-aphid symbiont abundance.…”

Section: Resultsmentioning

confidence: 75%

“…The mechanism of resistance is not known but requires that the bacterial symbiont be infected with the bacteriophage APSE, which encodes eukaryotic toxins hypothesized to harm A. ervi larvae developing within the aphid (17)(18)(19). Other HFS commonly found infecting pea aphids and associated with protective roles include Serratia symbiotica, which confers resistance to thermal stress, and Regiella insecticola, Spiroplasma, Rickettsia, and Rickettsiella viridis, which protect against an aphid-specific fungal pathogen, Pandora neoaphidis (8,(20)(21)(22)(23)(24).…”

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confidence: 99%

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Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa. We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by "hitchhiking" via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members.IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella. Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella. These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella. Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.KEYWORDS Hamiltonella defensa, PAXS, entomopathogenic fungi, heat stress, heritable symbionts, parasitoids, pea aphid resistance H eritable bacterial symbionts are ubiquitous in arthropod species, especially insects occupying terrestrial ecosystems (1). These heritable symbionts are usually maternally transmitted and cannot survive outside host tissues and consequently have limited s...

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Section: Resultsmentioning

confidence: 75%

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confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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“…However, these protective effects can differ markedly within a single symbiont 'species' [5,11,15]. Our study suggests that different strains of the protective symbiont H. defensa may be adapted to defend their host against different parasitoid families.…”

Section: Discussionmentioning

confidence: 80%

Evidence for specificity in symbiont-conferred protection against parasitoids

2015

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Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa, which in pea aphid (Acyrthosiphon pisum) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi, while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.

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Section: Introductionmentioning

confidence: 99%

“…Several bacterial symbionts of aphids confer protection against parasitoid wasps (Oliver et al, 2003(Oliver et al, , 2005Vorburger et al, 2009) and fungi (Scarborough et al, 2005;Lukasik et al, 2012). Spiroplasma bacteria confer protection against fungi in the pea aphid (Lukasik et al, 2012), against a nematode in Drosophila neotestacea (Jaenike et al, 2010b) and against a parasitoid wasp in Drosophila hydei . Wolbachia has been shown to increase resistance or tolerance of Drosophila and mosquitoes against RNA viruses and against the protozoan parasite Plasmodium (Hedges et al, 2008;Teixeira et al, 2008;Moreira et al, 2009;Osborne et al, 2009;Bian et al, 2010;Frentiu et al, 2010;Zele et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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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Unrelated facultative endosymbionts protect aphids against a fungal pathogen

Cited by 276 publications

References 48 publications

Aphid Heritable Symbiont Exploits Defensive Mutualism

Aphid Heritable Symbiont Exploits Defensive Mutualism

Evidence for specificity in symbiont-conferred protection against parasitoids

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

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