Phage loss and the breakdown of a defensive symbiosis in aphids

Weldon, Stephanie R.; Strand, Michael R.; Oliver, Kerry M.

doi:10.1098/rspb.2012.2103

Cited by 101 publications

(115 citation statements)

References 35 publications

Supporting

Mentioning

111

Contrasting

Unclassified

Order By: Relevance

“…tissue DNA kit (OMEGA Bio-Tek) by following the manufacturer's protocol. Fragments of the single-copy bacterial genes dnaK from H. defensa and gyrB from X-type, along with the dnaK gene from polyploid B. aphidicola, were amplified using quantitative PCR (32,(61)(62)(63). The X-type primers new to this study were ACG GAG GTG AGT ACC CGA AAA (forward) and ATC AGC GTT CAT CTC TCC CA (reverse).…”

Section: Methodsmentioning

confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

View full text Add to dashboard Cite

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...

show abstract

Section: Methodsmentioning

confidence: 99%

Aphid Heritable Symbiont Exploits Defensive Mutualism

Doremus

Oliver

2017

Appl Environ Microbiol

View full text Add to dashboard Cite

show abstract

“…Single-copy bacterial (dnaK) and phage (P28) genes were amplified using a Roche LightCycler to estimate the number of bacterial cells or phage genomic copies present in each aphid using primers, PCR cocktail, and reaction conditions as described above. Amplifications were analyzed with an external "absolute" standard curve produced from serial dilutions of 1E02 to 1E09 (34). Each qPCR run contained three standards and two negative controls to calibrate the external curve for each targeted gene.…”

Section: Methodsmentioning

confidence: 99%

“…In laboratory-reared Ac. pisum, vertical transmission rates of the common gammaproteobacterial facultative symbionts approach 100% (32)(33)(34). Inheritance failures under natural conditions and during the overwintering egg stage potentially influence symbiont frequencies, but rates of loss are unknown.…”

mentioning

confidence: 99%

Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids

Dykstra

Weldon

Martinez

et al. 2014

Appl Environ Microbiol

View full text Add to dashboard Cite

Many insects are associated with heritable symbionts that mediate ecological interactions, including host protection against natural enemies. The cowpea aphid, Aphis craccivora, is a polyphagous pest that harbors Hamiltonella defensa, which defends against parasitic wasps. Despite this protective benefit, this symbiont occurs only at intermediate frequencies in field populations. To identify factors constraining H. defensa invasion in Ap. craccivora, we estimated symbiont transmission rates, performed fitness assays, and measured infection dynamics in population cages to evaluate effects of infection. Similar to results with the pea aphid, Acyrthosiphon pisum, we found no consistent costs to infection using component fitness assays, but we did identify clear costs to infection in population cages when no enemies were present. Maternal transmission rates of H. defensa in Ap. craccivora were high (ca. 99%) but not perfect. Transmission failures and infection costs likely limit the spread of protective H. defensa in Ap. craccivora. We also characterized several parameters of H. defensa infection potentially relevant to the protective phenotype. We confirmed the presence of H. defensa in aphid hemolymph, where it potentially interacts with endoparasites, and performed real-time quantitative PCR (qPCR) to estimate symbiont and phage abundance during aphid development. We also examined strain variation of H. defensa and its bacteriophage at multiple loci, and despite our lines being collected in different regions of North America, they were infected with a nearly identical strains of H. defensa and APSE4 phage. The limited strain diversity observed for these defensive elements may result in relatively static protection profile for this defensive symbiosis.

show abstract

“…Protection by H. defensa is dependent on the presence of a bacteriophage, termed APSE (A. pisum Secondary Endosymbiont) [24], which carries putative toxin genes affecting eukaryotes [25,26]. Variation in toxin genes is correlated with variation in the strength of protection [11,27,28], while strains lacking the phage [25,28], or which carry phages with apparently inactivated toxin genes [29], provide no protection.…”

Section: Introductionmentioning

confidence: 99%

“…The partial sequences for P3 and P51 (989 bp and 497-813 bp, respectively) were then compared to published APSE sequences available in GenBank (see electronic supplementary material, tables S1 and S2, for details of comparison strains). A number of different phage strain types have been previously identified, only some of which have associated phenotypic data: strain APSE-3 has been found associated with strong protection against A. ervi and APSE-2 with partial protection [28]. Phylogenetic trees were constructed for P3 and P51 using maximum-likelihood methods implemented in PhyML v. 3.0 [52] using HKY and K80 substitution models, respectively.…”

Section: (D) Comparison Of Hamiltonella Defensa Andmentioning

confidence: 99%

Evidence for specificity in symbiont-conferred protection against parasitoids

2015

View full text Add to dashboard Cite

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.

show abstract

Phage loss and the breakdown of a defensive symbiosis in aphids

Cited by 101 publications

References 35 publications

Aphid Heritable Symbiont Exploits Defensive Mutualism

Aphid Heritable Symbiont Exploits Defensive Mutualism

Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids

Evidence for specificity in symbiont-conferred protection against parasitoids

Contact Info

Product

Resources

About