The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes
Authors: Makova Kateryna D. , Pickett Brandon D. , Harris Robert S. , Hartley Gabrielle A. , Cechova Monika , Pal Karol , Nurk Sergey , Yoo DongAhn , Li Qiuhui , Hebbar Prajna , McGrath Barbara C. , Antonacci Francesca , Aubel Margaux , Biddanda Arjun , Borchers Matthew , Bomberg Erich , Bouffard Gerard G. , Brooks Shelise Y. , Carbone Lucia , Carrel Laura , Carroll Andrew , Chang Pi-Chuan , Chin Chen-Shan , Cook Daniel E. , Craig Sarah J.C. , de Gennaro Luciana , Diekhans Mark , Dutra Amalia , Garcia Gage H. , Grady Patrick G.S. , Green Richard E. , Haddad Diana , Hallast Pille , Harvey William T. , Hickey Glenn , Hillis David A. , Hoyt Savannah J. , Jeong Hyeonsoo , Kamali Kaivan , Kosakovsky Pond Sergei L. , LaPolice Troy M. , Lee Charles , Lewis Alexandra P. , Loh Yong-Hwee E. , Masterson Patrick , McCoy Rajiv C. , Medvedev Paul , Miga Karen H. , Munson Katherine M. , Pak Evgenia , Paten Benedict , Pinto Brendan J. , Potapova Tamara , Rhie Arang , Rocha Joana L. , Ryabov Fedor , Ryder Oliver A. , Sacco Samuel , Shafin Kishwar , Shepelev Valery A. , Slon Viviane , Solar Steven J. , Storer Jessica M. , Sudmant Peter H. , Sweetalana  , Sweeten Alex , Tassia Michael G. , Thibaud-Nissen Françoise , Ventura Mario , Wilson Melissa A. , Young Alice C. , Zeng Huiqing , Zhang Xinru , Szpiech Zachary A. , Huber Christian D. , Gerton Jennifer L. , Yi Soojin V. , Schatz Michael C. , Alexandrov Ivan A. , Koren Sergey , O’Neill Rachel J. , Eichler Evan , Phillippy Adam M. 
Published: December 2023

AbstractApes possess two sex chromosomes—the male-specific Y and the X shared by males and females. The Y chromosome is crucial for male reproduction, with deletions linked to infertility. The X chromosome carries genes vital for reproduction and cognition. Variation in mating patterns and brain function among great apes suggests corresponding differences in their sex chromosome structure and evolution. However, due to their highly repetitive nature and incomplete reference assemblies, ape sex chromosomes have been challenging to study. Here, using the state-of-the-art experimental and computational methods developed for the telomere-to-telomere (T2T) human genome, we produced gapless, complete assemblies of the X and Y chromosomes for five great apes (chimpanzee, bonobo, gorilla, Bornean and Sumatran orangutans) and a lesser ape, the siamang gibbon. These assemblies completely resolved ampliconic, palindromic, and satellite sequences, including the entire centromeres, allowing us to untangle the intricacies of ape sex chromosome evolution. We found that, compared to the X, ape Y chromosomes vary greatly in size and have low alignability and high levels of structural rearrangements. This divergence on the Y arises from the accumulation of lineage-specific ampliconic regions and palindromes (which are shared more broadly among species on the X) and from the abundance of transposable elements and satellites (which have a lower representation on the X). Our analysis of Y chromosome genes revealed lineage-specific expansions of multi-copy gene families and signatures of purifying selection. In summary, the Y exhibits dynamic evolution, while the X is more stable. Finally, mapping short-read sequencing data from >100 great ape individuals revealed the patterns of diversity and selection on their sex chromosomes, demonstrating the utility of these reference assemblies for studies of great ape evolution. These complete sex chromosome assemblies are expected to further inform conservation genetics of nonhuman apes, all of which are endangered species.