Eighty million years of rapid evolution of the primate Y chromosome

Zhou, Yang; Zhan, Xiaoyu; Jin, Jiazheng; Zhou, Long; Bergman, Juraj; Li, Xuemei; Rousselle, Marjolaine; Belles, Meritxell Riera; Zhao, Lan; Fang, Miaoquan; Chen, Jiawei; Kuderna, Lukas F. K.; Marquès‐Bonet, Tomàs; Kitayama, H.; Hayakawa, Takashi; Yao, Yong‐Gang; Yang, Huanming; Cooper, David Neil; Qi, Xiao-Guang; Wu, Dong‐Dong; Schierup, Mikkel H.

doi:10.1038/s41559-022-01974-x

Cited by 16 publications

(18 citation statements)

References 97 publications

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“…Among Y ampliconic gene families, nine were described previously 6,14 (BPY2, CDY, DAZ, HSFY, RBMY, TSPY, VCY, FRG1, and GLUD1), with the majority functioning in spermatogenesis 6 , and four (FAM47AY, KRT18Y, TAF13Y, and TAF11L2Y) are described here for the first time (Fig. 6, Table S36).…”

Section: Protein-coding Genesmentioning

confidence: 85%

“…The Y chromosome of the common ancestor of great apes had likely already possessed ampliconic sequences and multi-copy gene families 15 , and all ape sex chromosomes share the same evolutionary strata 14 . Lineage-specific amplification and loss of ampliconic genes on the Y have been noted 14,15 . This progress notwithstanding, many questions about the evolution of great ape sex chromosomes have remained unanswered due to their incomplete assemblies.…”

Section: Introductionmentioning

confidence: 99%

“…The human Y was found to be more similar in terms of alignability and gene content to the gorilla Y than to the more closely related chimpanzee Y 13 . The Y chromosome of the common ancestor of great apes had likely already possessed ampliconic sequences and multi-copy gene families 15 , and all ape sex chromosomes share the same evolutionary strata 14 . Lineage-specific amplification and loss of ampliconic genes on the Y have been noted 14,15 .…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…The initial assemblies of the human and chimpanzee Ys revealed remarkable differences in structure and gene content 6,12 despite short divergence time, and an acceleration of substitution rates and gene loss on the Y was observed in the common ancestor of bonobo and chimpanzee 15 . The Y chromosome of the common ancestor of great apes had likely already possessed ampliconic sequences and multi-copy gene families 15 , and all ape sex chromosomes share the same evolutionary strata 14 , while experiencing lineage-specific amplification and loss of ampliconic genes 14,15 . This progress notwithstanding, the lack of complete ape sex chromosome assemblies prevented detailed inquiries into the evolution of ampliconic regions, palindromes, segmental duplications, structural variants, satellites, transposable elements (TEs), and gene copy number.…”

Section: Introductionmentioning

confidence: 99%

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The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

Makova,

Pickett,

Harris

et al. 2023

Preprint

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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.

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Section: Protein-coding Genesmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

Makova,

Pickett,

Harris

et al. 2023

Preprint

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Reduction of bitter taste receptor gene family in folivorous colobine primates relative to omnivorous cercopithecine primates

Hou,

Akhtar,

Hayashi

et al. 2024

Primates

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Bitter taste perception is important in preventing animals from ingesting potentially toxic compounds. Whole-genome assembly (WGA) data have revealed that bitter taste receptor genes (TAS2Rs) comprise a multigene family with dozens of intact and disrupted genes in primates. However, publicly available WGA data are often incomplete, especially for multigene families. In this study, we employed a targeted capture (TC) approach specifically probing TAS2Rs for ten species of cercopithecid primates with diverse diets, including eight omnivorous cercopithecine species and two folivorous colobine species. We designed RNA probes for all TAS2Rs that we modeled to be intact in the common ancestor of cercopithecids (“ancestral-cercopithecid TAS2R gene set”). The TC was followed by short-read and high-depth massive-parallel sequencing. TC retrieved more intact TAS2R genes than found in WGA databases. We confirmed a large number of gene “births” at the common ancestor of cercopithecids and found that the colobine common ancestor and the cercopithecine common ancestor had contrasting trajectories: four gene “deaths” and three gene births, respectively. The number of intact TAS2R genes was markedly reduced in colobines (25–28 detected via TC and 20–26 detected via WGA analysis) as compared with cercopithecines (27–36 via TC and 19–30 via WGA). Birth or death events occurred at almost every phylogenetic-tree branch, making the composition of intact genes variable among species. These results show that evolutionary change in intact TAS2R genes is a complex process, refute a simple general prediction that herbivory favors more TAS2R genes, and have implications for understanding dietary adaptations and the evolution of detoxification abilities.

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