Sex-specific changes in the aphid DNA methylation landscape.

Thomas C Mathers,Sam T Mugford,Gemy Kaithakottil,Lawrence Percival‐Alwyn,David Swarbreck,Cock Van Oosterhout,Saskia A Hogenhout,Yazhou Chen

doi:10.1111/mec.15216

Thomas C Mathers, Sam T Mugford + Show 6 more

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https://doi.org/10.1111/mec.15216

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Abstract

Aphids present an ideal system to study epigenetics as they can produce diverse, but genetically identical, morphs in response to environmental stimuli. Here, using whole genome bisulphite sequencing and transcriptome sequencing of the green peach aphid (Myzus persicae), we present the first detailed analysis of cytosine methylation in an aphid and investigate differences in the methylation and transcriptional landscapes of male and asexual female morphs. We found that methylation primarily occurs in a CG dinucleotide (CpG) context and that exons are highly enriched for methylated CpGs, particularly at the 3′ end of genes. Methylation is positively associated with gene expression, and methylated genes are more stably expressed than unmethylated genes. Male and asexual female morphs have distinct methylation profiles. Strikingly, these profiles are divergent between the sex chromosome and the autosomes; autosomal genes are hypomethylated in males compared to asexual females, whereas genes belonging to the sex chromosome, which is haploid in males, are hypermethylated. Overall, we found correlated changes in methylation and gene expression between males and asexual females, and this correlation was particularly strong for genes located on the sex chromosome. Our results suggest that differential methylation of sex‐biased genes plays a role in aphid sexual differentiation.

Highlights

Sexual dimorphism is widespread in the natural world, and such differences are often underpinned by genetic adaptations that reside on the sex chromosomes (Mank 2009; Rice 2006)
We considered the magnitude of sex bias, classifying genes as either moderately sex-biased (1.5 ≤ fold change (FC) < 10, for FAB or MB) or extremely sex-biased (FC ≥ 10, for FAB+ or MB+)
The male-biased expression is consistent with patterns of gene expression in the pea aphid (Purandare et al 2014) and other invertebrates such as Caenorhabditis (Thomas et al 2012; Albritton et al 2014) and Drosophila (Zhang et al 2007), which show a tendency towards an excess of malebiased genes

Summary

Introduction

Sexual dimorphism is widespread in the natural world, and such differences are often underpinned by genetic adaptations that reside on the sex chromosomes (Mank 2009; Rice 2006). Insects show a vast diversity of sex chromosome systems which range from the classical male heterogametic XY system in Drosophila, to ZW systems in Lepidoptera (Kaiser and Bachtrog 2010; Blackmon et al 2017). In some insect clades, such as grasshoppers, crickets and cockroaches, the original Y chromosome has been completely lost. In those species, the males carry a single X, whereas females are XX (Kaiser and Bachtrog 2010). The absence of diverged sex chromosomes poses a non-trivial evolutionary challenge; how can a single genome code for phenotypes that are so fundamentally different as those of males and females? The absence of diverged sex chromosomes poses a non-trivial evolutionary challenge; how can a single genome code for phenotypes that are so fundamentally different as those of males and females? One possible solution is that the genes are differentially expressed in the sexes (Papa et al 2017; Ellegren and Parsch 2007; Wright et al 2018; Charlesworth 2018), and various epigenetic mechanisms have been suggested that could facilitate such expression variation (Grath and Parsch 2016; Holoch and Moazed 2015; Allis and Jenuwein 2016)

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