Comparison of fitness traits and their plasticity on multiple plants for Sitobion avenae infected and cured of a secondary endosymbiont

Wang, Da; Shi, Xiaoqin; Dai, Peng; Liu, Deguang; Dai, Xinjia; Shang, Zheming; Ge, Zhaohong; Meng, Xiuxiang

doi:10.1038/srep23177

Cited by 24 publications

(37 citation statements)

References 52 publications

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“…This was confirmed by the birth rates of the treatment groups, which were significantly lower than that of the controls. In conclusion, R. insecticola may reduce the potential growth of S. avenae clones, and this is consistent with the findings of Wang et al 27,. suggesting a possibility of a cost action to harbor this secondary endosymbiont.…”

Section: Discussionsupporting

confidence: 93%

“…Wang et al 27. obtained the “curing of R. insecticola infected lines” through an oral administration of antibiotics, and they studied the change in the developmental time of 1 st to 4 th instar nymphs (DT1-DT4), the total developmental time of nymphs (DT5), and 10 d fecundity.…”

Section: Discussionmentioning

confidence: 99%

“…To examine the dynamic population parameters affected by endosymbionts, an appropriate study of the life history of aphids is essential. Wang et al 27. reported the life history of R. insecticola in S. avenae using antibiotics to selectively cure infected lines (the elimination of secondary symbionts using 100 μg ml −1 ampicillin, 50 μg ml −1 cefotaxime and 50 μg ml −1 gentomicin).…”

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confidence: 99%

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Ecological impact of a secondary bacterial symbiont on the clones of Sitobion avenae (Fabricius) (Hemiptera: Aphididae)

Luo

Meng

et al. 2017

Sci Rep

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Many insects harbor heritable endosymbionts, whether obligatory or facultative, and the role of facultative endosymbionts in shaping the phenotype of these species has become increasingly important. However, little is known about whether micro-injected endosymbionts can have any effects on aphid clones, which was measured using various ecological parameters. We examined the effects between symbiotic treatments and the vital life history traits generated by Regiella insecticola on the life table parameters of Sitobion avenae. The results showed that R. insecticola can decrease the intrinsic rate of increase (r), the finite rate of increase (λ) and birth rate and can increase the mean generation times (T) of S. avenae clones, suggesting that R. insecticola may decelerate the normal development of the hosts. No significant differences of these parameters were observed between the examined Sitobion avenae clones, and the symbiont treatment by genotype interaction affected only the net reproduction rate R 0 , pre-adult duration and total longevity but not the other parameters. Additionally, a population projection showed that R. insecticola decelerated the growth of the S. avenae clones. The evocable effects of R. insecticola on the S. avenae clones may have significant ramifications for the control of S. avenae populations under field/natural conditions. Many insect species harbor endosymbionts, which are indispensable to their survival and common reproduction. Because the hosts and their endosymbionts share a common fate, endosymbionts can often profoundly affect the ecology and evolution of their hosts. Among them, the endosymbionts in aphids are ideal targets for studying their role in ecological fitness 1 . In nature, almost all aphid species possess the primary endosymbiont Buchnera aphidicola, which belongs to the class γ-proteobacterium. B. aphidicola synthesizes essential amino acids and other nutrients that are ingested in very small quantities from restricted diets, such as plant phloem, for their host aphids 2-4 . Moreover, aphids can also be infected with one or more non-essential secondary endosymbionts belonging to distinct bacterial lineages 1 . For example, Regiella insecticola, Hamiltonella defensa and Serratia symbiotica belong to the class γ-proteobacterium, and Rickettsia and Spiroplasma belong to the class α-proteobacterium [5][6][7][8][9][10][11][12][13] . Secondary endosymbionts do not present in all aphid individuals, suggesting they are not generally required for the survival and reproduction of aphids. However, endosymbionts can significantly affect host aphid ecological fitness and behavior. In the past few decades, secondary endosymbionts have been found to confer benefits on the pea aphid Acyrthosiphon pisum (Harris), including resistance to heat shock (S.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Ecological impact of a secondary bacterial symbiont on the clones of Sitobion avenae (Fabricius) (Hemiptera: Aphididae)

Luo

Meng

et al. 2017

Sci Rep

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“…), and other studies reported negative fitness effects of this symbiont, for example, in the grain aphid, Sitobion avenae (Wang et al. ; Luo et al. ).…”

Section: Discussionmentioning

confidence: 85%

Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids*

et al. 2019

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The heritable endosymbiont Spiroplasma infects many insects and has repeatedly evolved the ability to protect its hosts against different parasites. Defenses do not come for free to the host, and theory predicts that more costly symbionts need to provide stronger benefits to persist in host populations. We investigated the costs and benefits of Spiroplasma infections in pea aphids (Acyrthosiphon pisum), testing 12 bacterial strains from three different clades. Virtually all strains decreased aphid lifespan and reproduction, but only two had a (weak) protective effect against the parasitoid Aphidius ervi, an important natural enemy of pea aphids. Spiroplasma‐induced fitness costs were variable, with strains from the most slowly evolving clade reaching higher titers and curtailing aphid lifespan more strongly than other strains. Some Spiroplasma strains shared their host with a second endosymbiont, Regiella insecticola. Although the result of an unfortunate handling error, these co‐infections proved instructive, because they showed that the cost of infection with Spiroplasma may be attenuated in the presence of Regiella. These results suggest that mechanisms other than protection against A. ervi maintain pea aphid infections with diverse strains of Spiroplasma, and that studying them in isolation will not provide a complete picture of their effects on host fitness.

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“…It's believed that facultative endosymbionts can enhance some biological and ecological traits for their host aphids, such as the frequency of sexual reproduction (Leonardo & Mondor, ; Simon et al, ), body coloration (Tsuchida et al, ), resistance to parasitoid wasps and pathogenic fungi (Oliver, Russell, Moran, & Hunter, ; Scarborough, Ferrari, & Godfray, ), and the capacity to withstand heat shock (Montllor, Maxmen, & Purcell, ; Russell & Moran, ). One of the most studied facultative symbionts in aphids is Hamiltonella defensa (Oliver et al, ; Vorburger, Gehrer, & Rodriguez, ; Wang et al, ). Some studies have shown that H. defensa can protect its host aphids (e.g., A. pisum and Aphis fabae ) against parasitoids to certain extents (Martinez, Weldon, & Oliver, ; Oliver et al, ; Schmid, Sieber, Zimmermann, & Vorburger, ; Vorburger et al, ), and the significance of its protective roles is dependent on specific H. defensa isolates and associated bacteriophage variants of APSE ( Acyrthosiphon pisum secondary endosymbiont; Degnan & Moran, ; Oliver, Degnan, Hunter, & Moran, ).…”

Section: Introductionmentioning

confidence: 99%

Effects of a presumably protective endosymbiont on life‐history characters and their plasticity for its host aphid on three plants

Liu

Zhang

et al. 2018

Ecology and Evolution

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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.

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Comparison of fitness traits and their plasticity on multiple plants for Sitobion avenae infected and cured of a secondary endosymbiont

Cited by 24 publications

References 52 publications

Ecological impact of a secondary bacterial symbiont on the clones of Sitobion avenae (Fabricius) (Hemiptera: Aphididae)

Ecological impact of a secondary bacterial symbiont on the clones of Sitobion avenae (Fabricius) (Hemiptera: Aphididae)

Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids*

Effects of a presumably protective endosymbiont on life‐history characters and their plasticity for its host aphid on three plants

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