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Transcriptome profiling of maternal stress-induced wing dimorphism in pea aphids.

ABSTRACT: Wing dimorphism, that is, wingless and winged forms, can be induced by maternal stress signals and is an adaptive response of aphids to environmental changes. Here, we investigated the ecological and molecular effects of three kinds of stress, namely crowding, predation, and aphid alarm pheromone, on wing dimorphism. These three stressors induced high proportion of up to 60% of winged morphs in offspring. Transcriptome analysis of stress-treated female aphids revealed different changes in maternal gene expression induced by the three stressors. Crowding elicited widespread changes in the expression of genes involved in nutrient accumulation and energy mobilization. Distinct from crowding, predation caused dramatic expression changes in cuticle protein (CP) genes. Twenty-three CP genes that belong to CP RR2 subfamily and are highly expressed in legs and embryos were greatly repressed by the presence of ladybird. By contrast, application of alarm pheromone, E-β-farnesene, caused slight changes in gene expression. The three factors shared a responsive gene, cuticle protein 43. This study reveals the adaptive response of aphids to environmental stresses and provides a rich resource on genome-wide expression genes for exploring molecular mechanisms of ecological adaptation in aphids.

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This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.55b2b15.

SUBMITTER: Hu L

PROVIDER: S-EPMC6822051 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Transcriptome profiling of maternal stress-induced wing dimorphism in pea aphids.

Hu Lin L Gui Wanying W Chen Bing B Chen Li L

Ecology and evolution 20191002 20

Wing dimorphism, that is, wingless and winged forms, can be induced by maternal stress signals and is an adaptive response of aphids to environmental changes. Here, we investigated the ecological and molecular effects of three kinds of stress, namely crowding, predation, and aphid alarm pheromone, on wing dimorphism. These three stressors induced high proportion of up to 60% of winged morphs in offspring. Transcriptome analysis of stress-treated female aphids revealed different changes in matern ...[more]

PMID: 31695892

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Project description:Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids' stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade-offs with other traits, such as reproduction or symbiont maintenance. Potential trade-offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross-generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host-by-symbiont interactions influenced fecundity. Stress on first-generation aphids had cross-generational impacts on second-generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts.

Project description:An important contributing factor to the evolutionary success of insects is nutritional association with microbial symbionts, which provide the host insects with nutrients lacking in their unbalanced diets. These symbionts are often compartmentalized in specialized cells of the host, the bacteriocytes. Even though bacteriocytes were first described more than a century ago, few studies have explored their dynamics throughout the insect life cycle and in response to environmental stressors. Here, we use the Buchnera aphidicola/pea aphid symbiotic system to study how bacteriocytes are regulated in response to nutritional stress throughout aphid development. Using artificial diets, we analyzed the effects of depletion or excess of phenylalanine or leucine, two amino acids essential for aphid growth and whose biosynthetic pathways are shared between the host and the symbiont. Bacteriocytes responded dynamically to those treatments, while other tissues showed no obvious morphological change. Amino acid depletion resulted in an increase in bacteriocyte numbers, with the extent of the increase depending on the amino acid, while excess either caused a decrease (for leucine) or an increase (for phenylalanine). Only a limited impact on survival and fecundity was observed, suggesting that the adjustment in bacteriocyte (and symbiont) numbers is sufficient to withstand these nutritional challenges. We also studied the impact of more extreme conditions by exposing aphids to a 24 h starvation period at the beginning of nymphal development. This led to a dramatic drop in aphid survival and fecundity and a significant developmental delay. Again, bacteriocytes responded dynamically, with a considerable decrease in number and size, correlated with a decrease in the number of symbionts, which were prematurely degraded by the lysosomal system. This study shows how bacteriocyte dynamics is integrated in the physiology of insects and highlights the high plasticity of these cells.

Dataset Information

Transcriptome profiling of maternal stress-induced wing dimorphism in pea aphids.

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Transcriptome profiling of maternal stress-induced wing dimorphism in pea aphids.

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