Facultative Symbiont Infections Affect Aphid Reproduction

Simon, Jean‐Christophe; Boutin, Sébastien; Tsuchida, Tsutomu; Koga, Ryuichi; Gallic, Jean-François Le; Frantz, Adrien; Outreman, Yannick; Fukatsu, Takema

doi:10.1371/journal.pone.0021831

Cited by 156 publications

(169 citation statements)

References 58 publications

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“…These are known to provide protection to their hosts against heat stress and parasitoid infection, respectively (27), but symbionts may be costly to maintain outside specific ecological conditions (28). Although the reduction in host fitness recorded here indicates a cost of infection to hosts, such costs are likely dependent on both the symbiont and host genotypes (6,7,37,38). However, recent work on Hamiltonella-infected aphids indicates that in the absence of parasitoid wasps, against which Hamiltonella can provide considerable protection, harboring the symbiont may be universally costly, regardless of genetic background, although the extent of these costs varies (7,38).…”

Section: Discussionmentioning

confidence: 82%

The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum

Laughton

Fan

Gerardo

2014

Appl Environ Microbiol

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b While many endosymbionts have beneficial effects on hosts under specific ecological conditions, there can also be associated costs. In order to maximize their own fitness, hosts must facilitate symbiont persistence while preventing symbiont exploitation of resources, which may require tight regulation of symbiont populations. As a host ages, the ability to invest in such mechanisms may lessen or be traded off with demands of other life history traits, such as survival and reproduction. Using the pea aphid, Acyrthosiphon pisum, we measured survival, lifetime fecundity, and immune cell counts (hemocytes, a measure of immune capacity) in the presence of facultative secondary symbionts. Additionally, we quantified the densities of the obligate primary bacterial symbiont, Buchnera aphidicola, and secondary symbionts across the host's lifetime. We found life history costs to harboring some secondary symbiont species. Secondary symbiont populations were found to increase with host age, while Buchnera populations exhibited a more complicated pattern. Immune cell counts peaked at the midreproductive stage before declining in the oldest aphids. The combined effects of immunosenescence and symbiont population growth may have important consequences for symbiont transmission and maintenance within a host population.

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Section: Discussionmentioning

confidence: 82%

The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum

Laughton

Fan

Gerardo

2014

Appl Environ Microbiol

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“…The lack of expected benefits identified in this study suggests that North American X-type is not a conditional mutualist like the other common aphid HFS. It is also unlikely that X-type invades pea aphid populations as a reproductive manipulator, as pea aphids primarily reproduce asexually, although some reproductive manipulation has been seen with Spiroplasma-infected pea aphids during their sexual phase (44). Preliminary transmission experiments in the lab found high vertical transmission rates (Ͼ99%) and no instances of horizontal (i.e., infectious) transmission, together indicating that X-type is primarily maternally transmitted, similar to other common pea aphid HFS (45).…”

Section: Discussionmentioning

confidence: 99%

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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“…For example, removal of a bacterial symbiont from the fungus Rhizopus microsporus completely eliminates vegetative growth by preventing production of sporangia or spores [1]. Among plants, the presence and identity of mycorrhizal fungal symbionts can change relative rates of seed production and vegetative replication of the host [2 -4], and numerous studies have demonstrated the effects of endosymbionts on basic reproductive processes in insects [5][6][7][8][9]. Evidence from symbiotic cnidarians reveals that loss of symbionts can reduce sexual reproduction [10,11], and a change in the symbiont complement can transform mutualistic partners to parasites [12].…”

Section: Introductionmentioning

confidence: 99%

Symbiotic state influences life-history strategy of a clonal cnidarian

2014

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Along the North American Pacific coast, the common intertidal sea anemone Anthopleura elegantissima engages in facultative, flexible symbioses with Symbiodinium muscatinei (a dinoflagellate) and Elliptochloris marina (a chlorophyte). Determining how symbiotic state affects host fitness is essential to understanding the ecological significance of engaging in such flexible relationships with diverse symbionts. Fitness consequences of hosting S. muscatinei, E. marina or negligible numbers of either symbiont (aposymbiosis) were investigated by measuring growth, cloning by fission and gonad development after 8.5-11 months of sustained exposure to high, moderate or low irradiance under seasonal environmental conditions. Both symbiotic state and irradiance affected host fitness, leading to divergent life-history strategies. Moderate and high irradiances led to a greater level of gonad development in individuals hosting E. marina, while high irradiance and high summer temperature promoted cloning in individuals hosting S. muscatinei and reduced fitness of aposymbiotic anemones. Associating with S. muscatinei may contribute to the success of A. elegantissima as a spatial competitor on the high shore: (i) by offsetting the costs of living under high temperature and irradiance conditions, and (ii) by promoting a high fission rate and clonal expansion. Our results suggest that basic lifehistory characteristics of a clonal cnidarian can be affected by the identity of the endosymbionts it hosts.

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Facultative Symbiont Infections Affect Aphid Reproduction

Cited by 156 publications

References 58 publications

The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum

The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum

Aphid Heritable Symbiont Exploits Defensive Mutualism

Symbiotic state influences life-history strategy of a clonal cnidarian

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