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, 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
Penn State University, University Park, PA, USA.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
bioRxiv. 2023 Dec 1:2023.11.30.569198. doi: 10.1101/2023.11.30.569198.
Apes 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.
猿类拥有两条性染色体——雄性特有的Y染色体以及雄性和雌性共有的X染色体。Y染色体对雄性生殖至关重要，其缺失与不育有关。X染色体携带对生殖和认知至关重要的基因。大型猿类交配模式和脑功能的差异表明它们的性染色体结构和进化存在相应差异。然而，由于其高度重复的性质和不完整的参考组装，猿类性染色体一直难以研究。在此，我们使用为端粒到端粒（T2T）人类基因组开发的最先进的实验和计算方法，为五种大型猿类（黑猩猩、倭黑猩猩、大猩猩、婆罗洲猩猩和苏门答腊猩猩）以及一种小型猿类——合趾猿，生成了无间隙、完整的X和Y染色体组装。这些组装完全解析了扩增子、回文和卫星序列，包括整个着丝粒，使我们能够理清猿类性染色体进化的复杂性。我们发现，与X染色体相比，猿类Y染色体在大小上差异很大，比对性低且结构重排水平高。Y染色体上的这种差异源于特定谱系扩增子区域和回文序列（在X染色体上物种间更广泛共享）的积累，以及转座元件和卫星序列的丰富（在X染色体上代表性较低）。我们对Y染色体基因的分析揭示了多拷贝基因家族的特定谱系扩张和纯化选择的特征。总之，Y染色体表现出动态进化，而X染色体更稳定。最后，对来自100多个大型猿类个体的短读测序数据进行定位，揭示了它们性染色体上的多样性和选择模式，证明了这些参考组装在大型猿类进化研究中的实用性。这些完整的性染色体组装有望进一步为非人类猿类的保护遗传学提供信息，所有非人类猿类均为濒危物种。
