Evidence for specificity in symbiont-conferred protection against parasitoids

McLean, Ailsa H. C.; Godfray, H. Charles J.

doi:10.1098/rspb.2015.0977

Cited by 92 publications

(139 citation statements)

References 66 publications

(105 reference statements)

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“…As seen in prior studies using H. defensa carrying different APSE variants, including APSE8, single infection with the present study's strain of H. defensa with APSE8 did not confer any protection against attack by the parasitoid P. pequodorum ( Fig. 3) (LRT, F H ϭ 0.011 and P ϭ 0.9155 [36]). …”

Section: Resultsmentioning

confidence: 48%

“…Indeed, in a separate study which controlled for aphid genotypic effects, we found no evidence that X-type rescued loss of H. defensa-based protection at high temperatures, nor did we find that X-type provided any protection against the wasp A. ervi as a single infection (33). However, several studies with aphids, including pea aphids, show that symbiont-based protection against parasitoids can be specialized to particular parasitoid species (34)(35)(36)(37), rendering it possible that X-type provides protection specifically against the only other parasitoid, Praon pequodorum, commonly attacking the pea aphid in North America (38). In European pea aphids, some X-type strains have been implicated in providing protection from thermal stress, as well as challenges by the wasp A. ervi and the fungal pathogen P. neoaphidis (39).…”

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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: 48%

mentioning

confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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“…It has been shown that the resistance requires the presence of a bacteriophage (Oliver et al, 2009) that carries genes for putative eukaryote toxins which are presumed to act against the developing parasitoid (Degnan & Moran, 2008a, 2008b. Hamiltonella defensa strains vary considerably in the protection they provide , and there is evidence of both parasitoid-species and parasitoid-genotype specificity (Rouchet & Vorburger, 2012;Asplen et al, 2014;McLean & Godfray, 2015). A recent population cage experiment using a model aphid-parasitoid food web demonstrated that the presence or absence of H. defensa in one of the aphid species can affect community stability and dynamics (Rothacher et al, 2016;Sanders et al, 2016).…”

Section: Parasitoidsmentioning

confidence: 99%

Cascading effects of herbivore protective symbionts on hyperparasitoids

McLean

Hrček

Parker

et al. 2017

Ecological Entomology

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Abstract. 1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity.2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids).3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species.4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid-parasitoid-hyperparasitoid interactions we studied.5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.

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“…Also, H. defensa-conferred resistance varies according to parasitoid species. (Mclean and Godfray, 2015). Finally, environmental factors such as heat may reduce the parasitoid resistance conferred by H.…”

Section: Hamiltonella Defensamentioning

confidence: 99%

“…The interrelation study between these factors become more prevalent in recent years, such as host plant, parasitoid and symbiont (Mclean and Godfray, 2015); aphid, host plant and symbiont (Peccoud et al, 2015;Zytynska et al, 2016); host plant, parasitoid, natural enemies, symbiont and environment (Smith et al, 2015). First, as described above regarding Arsenophonus, facultative symbionts may influence the adaptation and distribution of their hosts through the colonization of new plants and climatic regions (Henry et al, 2013).…”

Section: Symbionts Interactions With Biotic and Abiotic Environmentmentioning

confidence: 99%

Nine facultative endosymbionts in aphids. A review

Guo

Hatt

et al. 2017

Journal of Asia-Pacific Entomology

101

112

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Aphids are frequently engaged in mutualistic associations with endosymbionts.Symbionts are bacterial or fungal microorganisms that can be obligate or facultative to aphids. Research showed facultative (or secondary) symbionts have numerous effects on their host aphids such as resistance to heat shock, parasitoids and fungus etc., which may consequently promote a co-evolution between symbionts and hosts. However, this symbiotic relation may be affected by several factors, such as the ability of symbionts to spread from aphids to others within and across populations, and the cost of infections for hosts. Moreover, aphid-symbionts interactions may be affected by aphid living environment such as its host plant, the presence of natural enemies or the temperature. Here we firstly described the functions of nine facultative symbionts (Serratia symbiotica, Hamiltonella defensa, Regiella insecticola, Rickettsia, Rickettsiella, PAXS (pea aphid X-type symbiont), Spiroplasma, Wolbachia and Arsenophonus) studied in aphids one by one, and discussed the associations between these symbionts and aphids, plants and environment. We aim to have a better knowledge of the roles the facultative symbionts play in aphid biology, ecology and evolution, which we believe can provide new inspirations for aphid control.

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Evidence for specificity in symbiont-conferred protection against parasitoids

Cited by 92 publications

References 66 publications

Aphid Heritable Symbiont Exploits Defensive Mutualism

Aphid Heritable Symbiont Exploits Defensive Mutualism

Cascading effects of herbivore protective symbionts on hyperparasitoids

Nine facultative endosymbionts in aphids. A review

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