Pervasive epigenetic effects of Drosophila euchromatic transposable elements impact their evolution

Abstract

Transposable elements (TEs) are widespread genomic parasites, and their evolution has remained a critical question in evolutionary genomics. Here, we study the relatively unexplored epigenetic impacts of TEs and provide the first genome-wide quantification of such effects in D. melanogaster and D. simulans. Surprisingly, the spread of repressive epigenetic marks (histone H3K9me2) to nearby DNA occurs at >50% of euchromatic TEs, and can extend up to 20 kb. This results in differential epigenetic states of genic alleles and, in turn, selection against TEs. Interestingly, the lower TE content in D. simulans compared to D. melanogaster correlates with stronger epigenetic effects of TEs and higher levels of host genetic factors known to promote epigenetic silencing. Our study demonstrates that the epigenetic effects of euchromatic TEs, and host genetic factors modulating such effects, play a critical role in the evolution of TEs both within and between species.

DOI: http://dx.doi.org/10.7554/eLife.25762.001

eLife digest

The DNA inside an organism encodes all the instructions needed for the organism to develop and work properly. Organisms carefully organize and maintain their DNA (collectively known as the genome) so that the genetic information remains intact and the cell can understand the instructions. However, there are some pieces of DNA that are capable of moving around the genome. For example, pieces known as transposable elements can make new copies of themselves and jump into new locations in the genome. Most transposons do not appear to have any important roles, and in fact they are usually harmful to organisms. Despite this, transposons are present in the genomes of almost all species. The number of transposons in a genome varies greatly between individuals and species, but it is not clear why this is the case.

Organisms have evolved ways to limit the damage caused by transposons. For example, many cells package regions of DNA containing transposons into a tightly packed structure known as heterochromatin. However, this type of DNA packaging sometimes spreads to neighboring sections of DNA. This is a problem because cells are not usually able to read the information contained within heterochromatin. This means that transposons can prevent some instructions from being produced when they should be. Lee and Karpen used fruit flies to investigate to what extent transposons harm organisms by changing the way DNA is packaged, and whether this influences how transposons evolve.

The experiments show that that more than half of the transposons in fruit flies cause neighboring sections of DNA to be packaged into heterochromatin. This can negatively impact up to 20% of genes in the genome. As a result, transposons that have harmful effects on DNA packaging are more likely to be lost from the fly population during evolution than transposons that do not have harmful effects. Fruit fly species containing transposons that tend to package more neighboring sections of DNA into heterochromatin generally have fewer transposons than genomes containing less harmful transposons.

The findings of Lee and Karpen provide new insight as to why the numbers of transposons vary among organisms. The next challenge is to find out whether transposons that alter how DNA is packaged are also common in primates and other animals.

DOI: http://dx.doi.org/10.7554/eLife.25762.002