Centromere-associated retroelement evolution inDrosophila melanogasterreveals an underlying conflict

Abstract

ABSTRACTCentromeres are chromosomal regions essential for coordinating chromosome segregation during cell division. While centromeres are defined by the presence of a centromere-specific histone H3 variant rather than a particular DNA sequence, they are typically embedded in repeat-dense chromosomal genome regions. In many species, centromeres are associated with transposable elements, but it is unclear if these elements are selfish or if they play a role in centromere specification or function. Here we useDrosophila melanogasteras a model to understand the evolution of centromere-associated transposable elements.G2/Jockey-3is a non-LTR retroelement in theJockeyclade and the only sequence shared by all centromeres. We study the evolution ofG2/Jockey-3using short and long read population genomic data to infer insertion polymorphisms across the genome. We combine estimates of the age, frequency, and location of insertions to infer the evolutionary processes shapingG2/Jockey-3and its association with the centromeres. We find thatG2/Jockey-3is an active retroelement targeted by the piRNA pathway that is enriched in centromeres at least in part due to an insertion bias. We do not detect signatures of positive selection on anyG2/Jockey-3insertions that would suggest than individual copies are favored by natural selection. Instead, we infer that most insertions are neutral or weakly deleterious both inside and outside of the centromeres. Therefore,G2/Jockey-3evolution is consistent with it being a selfish genetic element that targets centromeres. We propose that targeting centromeres helps active retroelements escape host defenses, as the unique centromeric chromatin may prevent targeting by the host silencing machinery. At the same time, centromeric TEs insertions may be tolerated or even beneficial if they also contribute to the transcriptional and chromatin environment. Thus, we suspect centromere-associated retroelements likeG2/Jockey-3reflect a balance between conflict and cooperation at the centromeres.