Environmentally Selected Aphid Variants in Clonality Context Display Differential Patterns of Methylation in the Genome

Abstract

Heritability of acquired phenotypic traits is an adaptive evolutionary process that appears more complex than the basic allele selection guided by environmental pressure. In insects, the trans-generational transmission of epigenetic marks in clonal and/or sexual species is poorly documented. Aphids were used as a model to explore this feature because their asexual phase generates a stochastic and/or environment-oriented repertoire of variants. The a priori unchanged genome in clonal individuals prompts us to hypothesize whether covalent methyl DNA marks might be associated to the phenotypic variability and fitness selection. The full differential transcriptome between two environmentally selected clonal variants that originated from the same founder mother was mapped on the entire genomic scaffolds, in parallel with the methyl cytosine distribution. Data suggest that the assortments of heavily methylated DNA sites are distinct in these two clonal phenotypes. This might constitute an epigenetic mechanism that confers the robust adaptation of insect species to various environments involving clonal reproduction.

Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure

“…Under long-day conditions, it reproduces asexually by apomictic parthenogenesis (i.e., oocytes are parthenogenetically produced without meiosis or recombination). The pea aphid asexual phase generates a stochastic and/or environment-oriented repertoire of epigenetic variants with distinct behavioural and physiological traits (Dombrovsky et al 2009;Pasquier et al 2014). After acquisition, these epigenetic and phenotypic variants can be inherited across generations (de Vos et al 2010;Walsh et al 2010), and artificially selected (Andrade and Roitberg 1995;Pasquier et al 2014).…”

“…The pea aphid asexual phase generates a stochastic and/or environment-oriented repertoire of epigenetic variants with distinct behavioural and physiological traits (Dombrovsky et al 2009;Pasquier et al 2014). After acquisition, these epigenetic and phenotypic variants can be inherited across generations (de Vos et al 2010;Walsh et al 2010), and artificially selected (Andrade and Roitberg 1995;Pasquier et al 2014). Transgenerational plastic responses to environmental factors are common in aphids and play an important role in their life-cycle and population dynamics (Srinivasan and Brisson 2012;Sentis et al 2017b).…”

“…Moreover, this refractory phase can persist up to two aphid generations (Sutherland 1970), which suggests that exposure to stress can influence winged aphid frequencies for up to three generations with a high-winged frequency at the first generation followed by low-winged frequencies for the next two generations. Previous studies on molecular mechanisms reported that this extreme and discrete transgenerational phenotypic response (i.e., the production of winged offspring) is under the control of the ecdysone hormone and might involve alternative DNA methylation patterns at specific genome locations (Zera 2003;Brisson 2010;Pasquier et al 2014;Vellichirammal et al 2016;Vellichirammal et al 2017). Transgenerational plasticity in wing production thus provides an opportunity to study the evolution of a trait based on epigenetically inherited information.…”

Fear of predation alters clone-specific performance in phloem-feeding prey

“…1 ). Such induced aphid response to threat stimuli can be communicated amongst members of the clone both horizontally and vertically via maternal preconditioning of offspring 51 , 52 following hereditary and non-hereditary routes 31 , 52 , 53 . Inter-generational communication may be a strategy of insect prey to avoid risky plants; with evidence for the ability of sap-feeding insects to learn to avoid environmental risk 33 .…”

Paternal knockdown of tRNA (cytosine-5-)-methyltransferase (Dnmt2) increases offspring susceptibility to infection in red flour beetles

“…CpG methylation 3 . In insects, CpG methylation of DNA has been extensively studied 4,5 and is involved in many processes, such as caste determination and phase polyphenism [6][7][8][9][10] . However, this modification not only occurs on DNA, but also on a variety of RNAs 11 .…”