Transposable elements (TEs) are selfish genetic parasites that increase their copy number at the expense of host fitness. The 'success', or genome-wide abundance, of TEs differs widely between species. Deciphering the causes for this large variety in TE abundance has remained a central question in evolutionary genomics. We previously proposed that species-specific TE abundance could be driven by the inadvertent consequences of host-direct epigenetic silencing of TEs-the spreading of repressive epigenetic marks from silenced TEs into adjacent sequences. Here, we compared this TE-mediated local enrichment of repressive marks, or 'the epigenetic effect of TEs', in six species in the Drosophila melanogaster subgroup to dissect step-by-step the role of such effect in determining genomic TE abundance. We found that TE-mediated local enrichment of repressive marks is prevalent and substantially varies across and even within species. While this TE-mediated effect alters the epigenetic states of adjacent genes, we surprisingly discovered that the transcription of neighboring genes could reciprocally impact this spreading. Importantly, our multi-species analysis provides the power and appropriate phylogenetic resolution to connect species-specific host chromatin regulation, TE-mediated epigenetic effects, the strength of natural selection against TEs, and genomic TE abundance unique to individual species. Our findings point toward the importance of host chromatin landscapes in shaping genome evolution through the epigenetic effects of a selfish genetic parasite.
Keywords: D. melanogaster; chromatin; epigenetics; evolutionary biology; genome evolution; heterochromatin; population genetics; transposable element.
All the instructions required for life are encoded in the set of DNA present in a cell. It therefore seems natural to think that every bit of this genetic information should serve the organism. And yet most species carry parasitic ‘transposable’ sequences, or transposons, whose only purpose is to multiply and insert themselves at other positions in the genome. It is possible for cells to suppress these selfish elements. Chemical marks can be deposited onto the DNA to temporarily ‘silence’ transposons and prevent them from being able to move and replicate. However, this sometimes comes at a cost: the repressive chemical modifications can spread to nearby genes that are essential for the organism and perturb their function. Strangely, the prevalence of transposons varies widely across the tree of life. These sequences form the majority of the genome of certain species – in fact, they represent about half of the human genetic information. But their abundance is much lower in other organisms, forming a measly 6% of the genome of puffer fish for instance. Even amongst fruit fly species, the prevalence of transposable elements can range between 2% and 25%. What explains such differences? Huang et al. set out to examine this question through the lens of transposon silencing, systematically comparing how this process impacts nearby regions in six species of fruit flies. This revealed variations in the strength of the side effects associated with transposon silencing, resulting in different levels of perturbation on neighbouring genes. A stronger impact was associated with the species having fewer transposons in its genome, suggesting that an evolutionary pressure is at work to keep the abundance of transposons at a low level in these species. Further analyses showed that the genes which determine how silencing marks are distributed may also be responsible for the variations in the impact of transposon silencing. They could therefore be the ones driving differences in the abundance of transposons between species. Overall, this work sheds light on the complex mechanisms shaping the evolution of genomes, and it may help to better understand how transposons are linked to processes such as aging and cancer.
© 2022, Huang et al.