Centromeric transposable elements and epigenetic status drive karyotypic variation in the eastern hoolock gibbon.

Abstract

Great apes have maintained a stable karyotype with few large-scale rearrangements; in contrast, gibbons have undergone a high rate of chromosomal rearrangements coincident with rapid centromere turnover. Here, we characterize fully assembled centromeres in the eastern hoolock gibbon, Hoolock leuconedys (HLE), finding a diverse group of transposable elements (TEs) that differ from the canonical alpha-satellites found across centromeres of other apes. We find that HLE centromeres contain a CpG methylation centromere dip region, providing evidence that this epigenetic feature is conserved in the absence of satellite arrays. We uncovered a variety of atypical centromeric features, including protein-coding genes and mismatched replication timing. Further, we identify duplications and deletions in HLE centromeres that distinguish them from other gibbons. Finally, we observed differentially methylated TEs, topologically associated domain boundaries, and segmental duplications at chromosomal breakpoints, and thus propose that a combination of multiple genomic attributes with propensities for chromosome instability shaped gibbon centromere evolution.