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Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures.

ABSTRACT: Symbiosis is prevalent throughout the tree of life and has had a significant impact on the ecology and evolution of many bacteria and eukaryotes. The benevolence of symbiotic interactions often varies with the environment, and such variation is expected to play an important role in shaping the prevalence and distributions of symbiosis throughout nature. In this study, we examine how the fitness of aphids is influenced by infection with one of three maternally transmitted bacteria, 'Candidatus Serratia symbiotica', 'Candidatus Hamiltonella defensa' and 'Candidatus Regiella insecticola', addressing how symbiont benevolence varies with temperature. We find that the effects of these 'secondary' symbionts on Acyrthosiphon pisum depend on when and whether aphids are exposed to a brief period of heat shock. We also demonstrate that symbionts--even closely related isolates--vary in their effects on hosts. Our results indicate similar effects of S. symbiotica and H. defensa in conferring tolerance to high temperatures and a liability of R. insecticola under these same conditions. These findings reveal a role for heritable symbionts in the adaptation of aphids to their abiotic environments and add to an expanding body of knowledge on the adaptive significance of symbiosis.

SUBMITTER: Russell JA

PROVIDER: S-EPMC1560055 | biostudies-literature | 2006 Mar

REPOSITORIES: biostudies-literature

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Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures.

Russell Jacob A JA Moran Nancy A NA

Proceedings. Biological sciences 20060301 1586

Symbiosis is prevalent throughout the tree of life and has had a significant impact on the ecology and evolution of many bacteria and eukaryotes. The benevolence of symbiotic interactions often varies with the environment, and such variation is expected to play an important role in shaping the prevalence and distributions of symbiosis throughout nature. In this study, we examine how the fitness of aphids is influenced by infection with one of three maternally transmitted bacteria, 'Candidatus Se ...[more]

PMID: 16537132

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Project description:High-temperature events are evidenced to exert significant influence on the population performance and thermal biology of insects, such as aphids. However, it is not yet clear whether the bacterial symbionts of insects mediate the thermal tolerance traits of their hosts. This study is intended to assess the putative association among the chronic and acute thermal tolerance of two cereal aphid species, Rhopalosiphum padi (L.) and Sitobion avenae (F.), and the abundance of their bacterial symbionts. The clones of aphids were collected randomly from different fields of wheat crops and were maintained under laboratory conditions. Basal and acclimated CTmax and chronic thermal tolerance indices were measured for 5-day-old apterous aphid individuals and the abundance (gene copy numbers) of aphid-specific and total (16S rRNA) bacterial symbionts were determined using real-time RT-qPCR. The results reveal that R. padi individuals were more temperature tolerant under chronic exposure to 31 °C and also exhibited about 1.0 °C higher acclimated and basal CTmax values than those of S. avenae. Moreover, a significantly higher bacterial symbionts' gene abundance was recorded in temperature-tolerant aphid individuals than the susceptible ones for both aphid species. Although total bacterial (16S rRNA) abundance per aphid was higher in S. avenae than R. padi, the gene abundance of aphid-specific bacterial symbionts was nearly alike for both of the aphid species. Nevertheless, basal and acclimated CTmax values were positively and significantly associated with the gene abundance of total symbiont density, Buchnera aphidicola, Serratia symbiotica, Hamilton defensa, Regiella insecticola and Spiroplasma spp. for R. padi, and with the total symbiont density, total bacteria (16S rRNA) and with all aphid-specific bacterial symbionts (except Spiroplasma spp.) for S. avenae. The overall study results corroborate the potential role of the bacterial symbionts of aphids in conferring thermal tolerance to their hosts.

Project description:Bacterial symbionts associated with aphids are important for their ecological fitness. The corn leaf aphid, Rhopalosiphum maidis (Fitch), is one of the most damaging aphid pests on maize and has been reported to harbor Hamiltonella defensa and Regiella insecticola while the effects of the secondary symbionts (S-symbionts) on host ecology and primary symbiont Buchnera aphidicola remain unclear. Here, four aphid strains were established, two of which were collected from Langfang - Hebei Province, China, with similar symbiont pattern except for the presence of H. defensa. Two other aphid strains were collected from Nanning - Guangxi Province, China, with the same symbiont infection except for the presence of R. insecticola. Phylogenetic analysis and aphid genotyping indicated that the S-symbiont-infected and free aphid strains from the same location had identical genetic backgrounds. Aphid fitness measurement showed that aphid strain infected with H. defensa performed shortened developmental duration for 1st instar and total nymph stages, reduced aphid survival rate, offspring, and longevity. While the developmental duration of H-infected strains was accelerated, and the adult weight was significantly higher compared to the H-free strain. Infection with R. insecticola did not affect the aphid's entire nymph stage duration and survival rate. As the H-strain does, aphids infected with R. insecticola also underwent a drop in offspring, along with marginally lower longevity. Unlike the H-infected strain, the R-infected strain performed delayed developmental duration and lower adult weight. The B. aphidicola titers of the H-infected strains showed a steep drop during the aphid 1st to 3rd instar stages, while the augmentation of B. aphidicola titers was found in the R-infected strain during the aphid 1st to 3rd instar. Our study investigated for the first time the effect of the S-symbionts on the ecology fitness and primary symbiont in R. maidis, indicating that infection with secondary symbionts leads to the modulation of aphid primary symbiont abundance, together inducing significant fitness costs on aphids with further impact on environmental adaptation and trophic interactions.

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Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures.

Publications

Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures.

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