Germline hypomethylation shapes dynamic CpG reservoirs in ape genomes

CpG dinucleotides are essential substrates for DNA methylation and genome regulation, yet paradoxically, methylated CpGs are lost through deamination-associated mutations. How CpG-rich sequences persist and are replenished during evolution remains unresolved, as previous sequencing technologies left structurally complex regions inaccessible. Here, leveraging complete telomere-to-telomere ape genomes, we show that peri/centromeric satellites are reservoirs of hypomethylated CpGs in sperm, and likely oocytes. This peri/centromeric hypomethylation extends into adjacent euchromatin, revealing novel centromeric hypomethylation extension domains enriched for segmental duplications, recently duplicated genes, and testis- and brain-biased expression. More broadly, young structural variants are CpG-rich and germline-hypomethylated, whereas older sequences are methylated and CpG-depleted. These findings link rapidly evolving centromeric regions to distinctive germline epigenetic state, CpG evolution, and structural and transcriptomic evolutionary innovation.