Biotype-dependent secondary symbiont communities in sympatric populations of <i>Bemisia tabaci</i>

Chiel, Elad; Gottlieb, Yuval; Zchori-Fein, Einat; Mozes-Daube, Netta; Katzir, Nurit; Inbar, Moshe; Ghanim, Murad

doi:10.1017/s0007485307005159

Cited by 257 publications

(320 citation statements)

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“…The presence of genotypic tolerance suggests that we are generally underestimating costs to infection with X-type via selection of lines which produce enough offspring to experimentally examine. These findings make it even more surprising that X-type can infect up to 40% of individuals in pea aphid populations (9).…”

Section: Discussionmentioning

confidence: 99%

“…Alternatively, heritable symbionts can invade populations by manipulating host reproduction to favor infected females (6,7). Moreover, individual hosts are often infected with multiple inherited symbionts and antagonistic or synergistic interactions between superinfecting symbionts may enhance or reduce mutualistic services or costs, influencing symbiont spread within the host population (8)(9)(10). Instances of heritable pathogens are expected to be exceedingly rare (1), yet under some conditions, a heritable symbiont that was neither providing conditional benefits nor manipulating host reproduction could spread by "hitchhiking" alongside a beneficial symbiont (11).…”

mentioning

confidence: 99%

“…The propensity of X-type to occur only as a superinfection suggests that it may act synergistically by improving the performance of superinfected aphids, either by providing distinct benefits or by enhancing those of H. defensa. Alternatively, X-type may deploy a cheating strategy and spread by "hitchhiking" with the defensive mutualist H. defensa (4,9).…”

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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: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

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“…As mentioned above, it is unclear whether and why different symbiont complements are favoured in these host-specialized populations [54][55][56][57]. In B. tabaci, the different biotypes of this phytophagous insect are all associated with different symbiotic communities [97,101]. Unfortunately, the effects of these symbionts are not known, but this situation may suggest that the differentiation of this species complex has been, and is still, influenced by these communities.…”

Section: Insects As Symbiotic Communitiesmentioning

confidence: 99%

Bacterial symbionts in insects or the story of communities affecting communities

Ferrari

Vavre

2011

Phil. Trans. R. Soc. B

303

280

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Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.

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“…Buchnera, Hamiltonella, Rickettsia, Arsenophonus, Regiella, Serratia) which provide essential amino acids and may be involved in biotype formation and aphid defense (Ruggle and Gutierrez 1995;Birkle and Douglas 1999;Moran and Wernegreen 2000;Wille and Hartman 2009;Oliver et al 2010). These endosymbionts have been associated with different biotypes or host-races of insects, presumably because of the different nutrients and amino acids afforded by different hosts (Simon et al 2003;Chiel et al 2007). For example, Ruggle and Gutierrez (1995) indicated virulence to Lucerne (alfalfa) varieties is symbiont based.…”

Section: Genetic Basis For Biotype Evolutionmentioning

confidence: 99%