Abstract
The invasive harlequin ladybird Harmonia axyridis is a textbook example of polymorphism and polyphenism as the temperature during egg development determines the frequency of melanic morphs and the number and size of black spots in nonmelanic morphs. Recent concepts in evolutionary biology suggest that epigenetic mechanisms can translate environmental stimuli into heritable phenotypic changes. To investigate whether epigenetic mechanisms influence the penetrance and expressivity of colour morphs in H. axyridis, we used RNA interference to silence key enzymes required for DNA methylation and histone modification. We found that neither of these epigenetic mechanisms affected the frequency of different morphs, but there was a significant impact on life-history traits such as longevity and fecundity. Strikingly, we found that silencing the gene encoding for DNA methyltransferase 1 associated protein 1 (DMAP1) severely reduced female fecundity, which correlated with an abundance of degenerated ovaries in DMAP1-knockdown female beetles. Finally, we observed significant differences in DMAP1 expression when we compared native and invasive H. axyridis populations with a biocontrol strain differing in egg-laying capacity, suggesting that the DNA methyltransferase 1-DMAP1 complex may influence the invasive performance of this ladybird.
Highlights
Individuals of the same species can often be assigned to one of several distinct phenotypes, a phenomenon known as polymorphism when the variation depends on genetic differences and polyphenism when an identical genome can give rise to different phenotypes according to the environment (Simpson et al, 2011)
A very recent study combined whole-genome sequencing, population-based genome-wide association studies, gene expression, and functional analyses to determine that the transcription factor Pannier regulates melanic pattern polymorphism in H. axyridis and that highly variable discrete colour forms in natural populations result from cisregulatory allelic variation of a single gene (Gautier et al, 2018)
The mechanism that underlies polyphenism is unclear, but epigenetic mechanisms may explain some of the features of this phenomenon, such as the ability of environmental pressure in one generation to affect the phenotype of later generations (Glastad et al, 2019; Simpson et al, 2011)
Summary
Individuals of the same species can often be assigned to one of several distinct phenotypes, a phenomenon known as polymorphism when the variation depends on genetic differences and polyphenism when an identical genome can give rise to different phenotypes according to the environment (Simpson et al, 2011). Recent concepts predict that epigenetic mechanisms control transcriptional reprogramming resulting in phenotypic plasticity (Flores et al, 2013) To test this hypothesis, we investigated whether the frequency of H. axyridis colour morphs in response to temperature is mediated by epigenetic mechanisms. DNA methylation is mediated by enzymes known as DNA methyltransferases (DNMTs), which catalyse the addition of methyl groups to cytidine residues and favour the formation of compact and inaccessible chromatin, generally blocking the interaction between DNA and transcription factors (Jurkowska et al, 2011) In this process the DNA methyltransferase 1 associated binding protein 1 (DMAP1) is the key activator of DNMT1, as the loss of this protein results in hypomethylation (Lee et al, 2010; Rountree et al, 2010). We found that the phenotypic plasticity of H. axyridis was not affected by the double-stranded RNA (dsRNA) treatment of any of these target genes, but we observed a striking and unexpected impact on life-history parameters, which we investigated in the context of differences in gene expression between invasive, non-invasive and laboratory-bred populations
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