Hamiltonella defensa is well known for its protective roles against parasitoids for its aphid hosts, but its functional roles in insect‐plant interactions are less understood. Thus, the impact of H. defensa infections on life‐history characters and the underlying genetic variation for the grain aphid, Sitobion avenae (Fabricius), was explored on three plants (i.e., wheat, oat, and rye). Compared to cured lines, H. defensa infected lines of S. avenae had lower fecundity on wheat and oat, but not on rye, suggesting an infection cost for the aphid on susceptible host plants. However, when tested on rye, the infected lines showed a shorter developmental time for the nymphal stage than corresponding cured lines, showing some benefit for S. avenae carrying the endosymbiont on resistant host plants. The infection of H. defensa altered genetic variation underlying its host S. avenea’s life‐history characters, which was shown by differences in heritabilities and genetic correlations of life‐history characters between S. avenae lines infected and cured of the endosymbiont. This was further substantiated by disparity in G‐matrices of their life‐history characters for the two types of aphid lines. The G‐matrices for life‐history characters of aphid lines infected with and cured of H. defensa were significantly different from each other on rye, but not on oat, suggesting strong plant‐dependent effects. The developmental durations of infected S. avenae lines showed a lower plasticity compared with those of corresponding cured lines, and this could mean higher adaptability for the infected lines.Overall, our results showed novel functional roles of a common secondary endosymbiont (i.e., H. defensa) in plant‐insect interactions, and its infections could have significant consequences for the evolutionary ecology of its host insect populations in nature.
The development of biotypes of the cereal aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), was initially found only on wheat, but barley can also be critical in the process. To address this issue, S. avenae clones were collected on barley and wheat, genotyped with six microsatellite markers, and tested with 58 wheat/barley varieties. Based on the virulence response profiles on different resistant wheat/barley varieties and three susceptible controls, six biotypes of S. avenae were identified. We developed a new system to distinguish between S. avenae biotypes by using only five barley/wheat varieties (i.e., barley: Dulihuang, Zaoshu No.3, Xiyin No.2; wheat: Zhong 4 wumang, 186-TM12-34). The unique virulence profiles of different S. avenae biotypes were further verified by testing their life-history traits (i.e., 10-d fecundity and total developmental time of nymphs) on the abovementioned five barley/wheat varieties. Among all the identified biotypes, biotype 1 was predominant, occupying over 82% of the total in each province. Biotype 5 was found only in Xinjiang, whereas biotype 6 occurred only in Zhejiang. The principal coordinate analysis with microsatellite data suggested apparently low genetic differentiation between biotypes 1 and 2. In most cases, extents of genetic divergence between different S. avenae biotypes could reflect differences in virulence response profiles of these biotypes, implying a genetic component for evolutionary relationships among these biotypes. Our study provides insights into the development and evolution of aphid biotypes, and a firm basis for clarifying the underlying genetic and evolutionary mechanisms.
The English grain aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), is a significant pest of cereal crops, but molecular factors and mechanisms that underpin its ability to develop differential biotypes on variable host plants are still not well understood. In this study, we investigated the interactions between two plant secondary metabolites (i.e., gramine and gallic acid) and three glutathione S-transferases (GSTs) of S. avenae. Using artificial diets complemented or not with one of these two plant compounds, we found that gramine had relatively stronger negative effects on fitness of S. avenae biotype 3 (adapted to barley), and gallic acid on that of biotype 4 (adapted to wheat). Gramine significantly induced overexpression of SaveGST1 and SaveGST2 in biotype 4, but not in biotype 3. Gramine also reduced SaveGST3 expression in biotype 4, but not in biotype 3, suggesting biotypespecific effect of GSTs' regulation. In the treatments with gallic acid, the overexpression of SaveGST1, but not SaveGST2 or SaveGST3, was significantly induced in both biotypes, suggesting a critical role of SaveGST1 in detoxification of phenolic compounds such as gallic acid. The total constitutive GST activity was much higher in biotype 4 than in biotype 3. Significant increase in GST activity was obtained by the addition of both secondary metabolites in biotype 4, but not in biotype 3, showing significantly higher expression plasticity of GSTs in biotype 4. Thus, both constitutive and induced expression of GSTs could affect the adaptability of S. avenae on plants with variable secondary compounds, and thus contribute to the divergence of biotypes in this aphid species.
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