Centromere-associated retroelement evolution in Drosophila melanogaster reveals an underlying conflict

Centromeres 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 called CENP-A rather than a particular DNA sequence, they are typically embedded in repeat-dense and heterochromatic chromosomal genome regions. In many species, centromeres are associated with transposable elements but it is unclear if these elements are selfish and target centromeres for insertion or if they play a role in centromere specification and function. Here we use Drosophila melanogaster as a model to understand the evolution of centromere-associated transposable elements. G2/Jockey-3 is a non-LTR retroelement in the Jockey clade and the only sequence shared by all centromeres. We study the evolution of G2/Jockey-3 using 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 shaping G2/Jockey-3 and its association with the centromeres. We find that G2/Jockey-3 is an active retroelement that is targeted by the piRNA pathway. Our results suggest that G2-Jockey-3 is highly enriched in centromeres at least in part due to an insertion bias. We do not detect any signature of positive selection on any G2/Jockey-3 insertions that would suggest than individual insertions 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-3 evolution is consistent with it being a selfish genetic element that targets centromeres. We suspect targeting centromeres for insertion helps active retroelements like G2/Jockey-3 escape host defenses, as the unique centromeric chromatin may prevent targeting by the host silencing machinery. On the other hand, centromeric TEs insertions may be tolerated or even beneficial if they also contribute to the right transcriptional and chromatin environment. Thus, we suspect centromere-associated retroelements like G2/Jockey-3 reflect a balance between conflict and cooperation at the centromeres.