Multiple phenotypes conferred by a single insect symbiont are independent

Abstract

Many microbial symbionts have multiple phenotypic consequences for their animal hosts. However, the ways in which different symbiont-mediated phenotypes combine to affect fitness are not well understood. We investigated whether there are correlations between different symbiont-mediated phenotypes. We used the symbiont Spiroplasma , a striking example of a bacterial symbiont conferring diverse phenotypes on insect hosts. We took 11 strains of Spiroplasma infecting pea aphids ( Acyrthosiphon pisum ) and assessed their ability to provide protection against the fungal pathogen Pandora neoaphidis and the parasitoids Aphidius ervi and Praon volucre . We also assessed effects on male offspring production for five of the Spiroplasma strains. All but one of the Spiroplasma strains provided very strong protection against the parasitoid P. volucre . As previously reported, variable protection against P. neoaphidis and A. ervi was also present; male-killing was likewise a variable phenotype. We find no evidence of any correlation, positive or negative, between the different phenotypes, nor was there any evidence of an effect of symbiont phylogeny on protective phenotype. We conclude that multiple symbiont-mediated phenotypes can evolve independently from one another without trade-offs between them.

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

“…Recent findings have implicated Spiroplasma as an anti-parasitoid defender, with resistance to A. ervi being encoded by a modest number of European strains [ 90 , 91 ]. And in our final model for this symbiont ( Table 2 ), we found a positive correlation between its frequency and the proportion of aphids mummifying from A. ervi parasitism (z-value: 3.561; p -value: 0.02884).…”

“…Prior studies have suggested varying ecological roles for these additional pea aphid symbionts, including defense against the fungal pathogen Pandora neoaphidis ( Regiella , Rickettsia , Rickettsiella , and some strains of Spiroplasma— e.g., [ 86 , 87 ]), thermotolerance ( Serratia and Rickettsia , e.g., [ 74 , 88 , 89 ]), and possible further defense against Aphidius ervi or other parasitoids ( Spiroplasma [ 90 , 91 ]). Fukatsuia symbionts have been shown to impact all three phenotypes in European pea aphids [ 92 , 93 ].…”

Intraspecific variation in immune gene expression and heritable symbiont density

“…Spiroplasma and Serratia symbiotica did not alter expression of either gene, but two strains of Hamiltonella defensa significantly downregulated PO1 expression but not hemocytin (post-hoc tests, S2 Table and Fig 1D and 1E , right panels). Like Regiella , the specific strain of Spiroplasma (.161) we used was found in previous work to protect against fungal pathogens [ 49 ], but Serratia and Hamiltonella have been shown not to influence fungal resistance [ 36 , 50 , 51 ]. These results therefore suggest that the changes we identify in immune gene expression do not reflect the mechanism by which Regiella confers protection to aphids against fungal pathogens, which is currently unknown.…”

Variation in intrinsic resistance of pea aphids to parasitoid wasps: A transcriptomic basis

“…Pea aphids reproduce by apomictic parthenogenesis under long photoperiod conditions (16h:8h light: dark cycle) allowing us to maintain genetically-identical stocks in the laboratory for extended periods of time. Microsatellite typing was used to verify that the lines used in experiments were correctly assigned to the 'Medicago sativa' biotype [20,21], and to ensure that the lines used were genetically distinct from one another. We screened aphids for the seven known pea aphid facultative symbionts using diagnostic PCR [22], and we then cleared all such symbionts using oral administration of specific antibiotics which do not impact the aphid primary PLOS ONE symbiont, Buchnera aphidicola, as described in [23].…”

“…We used the results of the above experiments to choose two groups of contrasting aphids (each comprising three aphid lines): one group was vulnerable to A. ervi (genotypes C218, C215 and C681) and the other highly resistant (genotypes C308, C207, and C238). We ensured that the lines selected were genetically distinct based on the microsatellite sequencing [20,21] and did not contain pairs of highly-related genotypes within groups. In order to keep conditions as similar as possible between treatments, we used virgin female wasps for this experiment (as wasps are haplodipoid, this means all eggs laid will be male).…”