Transposable elements drive phenotypic variation and shape the response to environmental changes in Drosophila melanogaster
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Transposable elements (TEs) are ubiquitous repetitive DNA sequences that can mobilise within genomes and may modulate gene expression in an environment-dependent manner. TEs and the safeguarding epigenetic machinery targeting them, can be tuned by environmental fluctuations to influence gene expression by inducing genomic, epigenetic, and transcriptomic changes. Yet, the degree to which TE-driven molecular diversity translate into inter-individual phenotypic variation vs accumulating without any phenotypic consequences remains unclear. Here, we used five populations of genetically engineered Drosophila melanogaster flies that carry variable TE content but share an otherwise identical genetic background to test the phenotypic consequences of the early stages of TE accumulation. Phenotypic screenings across 17 traits (fertility-related traits, life-history traits and stress resistance tests) revealed significant differences between the populations (e.g. reduced hatchability). We also observed a notable increase in intra-population phenotypic variation for the heavily TE-burdened populations across a wide panel of traits. These results suggest considerable TE-driven inter- and intra-population phenotypic variation. Further investigation revealed that variable TE contents can influence the response to environmental changes, positioning TEs as drivers of environmentally-induced phenotypic variation in a system deprived of other sources of genetic variation. These results provide empirical evidence that TEs contribute to the heterogeneity of the environmental response and therefore represent an underlying mechanism of phenotypic variation.
Significant statement
The molecular mechanisms underlying phenotypic variation and variation in the environmental response continue to be a central question in evolutionary biology. Leveraging a biological system composed of Drosophila melanogaster populations containing varying levels of transposable elements (TEs), which are repetitive and widespread genomic elements, within an otherwise identical genetic background, we demonstrate the influence of TEs in generating phenotypic variation. By employing this innovative system to isolate the specific contributions of TEs, we provide evidence for their role as drivers of both phenotypic variability and divergence of the environmental response. Such results show that, rather than being largely neutral or silenced through epigenetic mechanisms, TE accumulation can contribute to measurable phenotypic diversity and thus provide heritable variation that selection can act upon.
