Abstract
Complex quantitative traits, like size and behaviour, are a pervasive feature of natural populations. Quantitative trait variation is the product of both genetic and environmental factors, yet little is known about the mechanisms through which their interaction generates this variation. Epigenetic processes, such as DNA methylation, can mediate gene-by-environment interactions during development to generate discrete phenotypic variation. We therefore investigated the developmental role of DNA methylation in generating continuous size variation of workers in an ant colony, a key trait associated with division of labour. Here we show that, in the carpenter ant Camponotus floridanus, global (genome-wide) DNA methylation indirectly regulates quantitative methylation of the conserved cell-signalling gene Epidermal growth factor receptor to generate continuous size variation of workers. DNA methylation can therefore generate quantitative variation in a complex trait by quantitatively regulating the transcription of a gene. This mechanism, alongside genetic variation, may determine the phenotypic possibilities of loci for generating quantitative trait variation in natural populations.
Highlights
Complex quantitative traits, like size and behaviour, are a pervasive feature of natural populations
Studies in the wild and in the lab spanning more than 100 years have identified nutrition levels and social interactions as critical environmental factors that influence the final size of workers during larval development[16,17,18,19]
By linking a continuous distribution in a trait in a natural population with a continuous distribution of DNA methylation states in a single gene, our study provides an epigenetic mechanism for generating quantitative variation in organismal phenotypes
Summary
Like size and behaviour, are a pervasive feature of natural populations. Knockdown of a DNA methylating enzyme (Dnmt3) in adult honeybee fat tissue affects alternative splicing[34], whereas knockdown of this enzyme in developing honeybee larvae results in the appearance of queen-like morphologies and a change in transcription levels of several types of genes, including those involved in growth and metabolism[7]. One of these growth-regulating genes Target of rapamycin (Tor) is more methylated[33] and is expressed at lower levels[35] in developing workers than in queens. Knockdown of tor in queen-destined larvae results in adults with worker characteristics[35], indicating that gene body methylation is involved in repressing the expression of Tor in workers
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