Abstract
While ecological adaptation in insects can be reflected by plasticity of phenotype, determining the causes and molecular mechanisms for phenotypic plasticity (PP) remains a crucial and still difficult question in ecology, especially where control of insect pests is involved. Oedaleus asiaticus is one of the most dominant pests in the Inner Mongolia steppe and represents an excellent system to study phenotypic plasticity. To better understand ecological factors affecting grasshopper phenotypic plasticity and its molecular control, we conducted a full transcriptional screening of O. asiaticus grasshoppers reared in four different grassland patches in Inner Mongolia. Grasshoppers showed different degrees of PP associated with unique gene expressions and different habitat plant community compositions. Grasshopper performance variables were susceptible to habitat environment conditions and closely associated with plant architectures. Intriguingly, eco-transcriptome analysis revealed five potential candidate genes playing important roles in grasshopper performance, with gene expression closely relating to PP and plant community factors. By linking the grasshopper performances to gene profiles and ecological factors using canonical regression, we first demonstrated the eco-transcriptomic architecture (ETA) of grasshopper phenotypic traits (ETAGPTs). ETAGPTs revealed plant food type, plant density, coverage, and height were the main ecological factors influencing PP, while insect cuticle protein (ICP), negative elongation factor A (NELFA), and lactase-phlorizin hydrolase (LCT) were the key genes associated with PP. Our study gives a clear picture of gene-environment interaction in the formation and maintenance of PP and enriches our understanding of the transcriptional events underlying molecular control of rapid phenotypic plasticity associated with environmental variability. The findings of this study may also provide new targets for pest control and highlight the significance of ecological management practice on grassland conservation.
Highlights
A fundamental question in evolutionary biology is how phenotypic variation is created within a population
Vegetation height was highest in S. krylovii type (Sk), which was significantly different from Cs, L. chinensis type (Lc), and A. frigida type (Af) (F = 63.56, df = 19, P < 0.0001)
From the grasshopper-genes-plant communities (Figure 3C), the results show that expression levels of lactase-phlorizin hydrolase (LCT), Aper-1, and negative elongation factor A (NELFA) negatively related to overall grasshopper performance, while expression of Mpv17/PMP22 positively related to overall performance
Summary
A fundamental question in evolutionary biology is how phenotypic variation is created within a population. This topic is important because phenotypic variation is a raw resource for selection (Whitman and Agrawal, 2009); that is, the environment selects among phenotypes. Phenotypic variation derives mostly from two sources: genetic variation and phenotypic plasticity (PP) (Harrelson and Valentino, 2013; Lea, 2017; Ziv et al, 2017). Selection can hypothetically occur in minutes as when a sudden, extreme environmental event instantly eliminates all individuals not phenotypically and genetically resistant to the lethal factor. The rapid creation of phenotypic diversity via phenotypic plasticity is of great importance both for individual fitness and survival and for evolutionary biology
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