Telomere-to-telomere assemblies uncover secrets of ape sex chromosomes Maintenance of genome integrity during DNA replication

Evolution of ape sex chromosomes has remained enigmatic due to their highly repetitive nature and incomplete reference assemblies (particularly for the Y). Here we generated gapless, telomere-to-telomere assemblies of the X and Y chromosomes for all extant great ape species—chimpanzee, bonobo, gorilla, Bornean and Sumatran orangutans—and for an outgroup lesser ape, the siamang. To achieve this, we utilized state-of-the-art experimental and computational methods developed for deciphering the human T2T genome. These assemblies completely resolved ampliconic and satellite sequences, and allowed us to untangle ape sex chromosome evolution in unprecedented detail, leading to the following results. First, despite the divergence time of less than 18 million years, only 12-26% of non-human ape Y sequences align to the human Y, compared to 84-97% of non-human ape X sequences aligning to the human X. Second, depending on species, segmental duplications represent 21-53% of ape Y assemblies, compared to only 3.9-6.0% of ape X assemblies. Third, ampliconic sequences constitute 8.7-46% of ape Y assemblies, compared to only 0.15-1.1% of ape X assemblies. Most of such sequences on the Y are species-specific. Fourth, repeats account for 71-85% of ape Y assemblies compared to 57-64% of ape X assemblies. Our analyses indicate a remarkably dynamic evolution on the largely non-recombining Y chromosome, in contrast to a more stable evolution on the X chromosome. As the Y harbors regions important for fertility, our research will inform future studies of conservation genetics of non-human apes, all of which are endangered species.