Dynamic evolution of great ape Y chromosomes

Abstract

The mammalian male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive and haploid nature, it is frequently absent from genome assemblies and remains enigmatic. The Y chromosomes of great apes represent a particular puzzle: their gene content is more similar between human and gorilla than between human and chimpanzee, even though human and chimpanzee shared a more recent common ancestor. To solve this puzzle, here we constructed a dataset including Ys from all extant great ape genera. We generated assemblies of bonobo and orangutan Ys, from short and long sequencing reads, and aligned them with the publicly available human, chimpanzee and gorilla Y assemblies. Analyzing this dataset, we found that the genus Pan , including chimpanzee and bonobo, experienced accelerated substitution rates. Additionally, Pan also exhibited elevated gene death rates. These observations are consistent with high levels of sperm competition in Pan . Furthermore, we inferred that the great ape common ancestor already possessed multi-copy sequences homologous to most human and chimpanzee palindromes. Nonetheless, each species also acquired distinct ampliconic sequences. We also detected increased chromatin contacts between and within palindromes (from Hi-C data), likely facilitating gene conversion and structural rearrangements. Moreover, our ENCODE data analysis suggested that Y palindromes exist to promote gene conversion preventing degradation of not only genes, as is commonly believed, but also gene regulatory sites. Our results highlight the dynamic mode of Y chromosome evolution, and open avenues for studies of male-specific dispersal in endangered great ape species.

The complex Y‐chromosomal history of gorillas

“…Morphological evidence also suggests historical gene flow among the species (Ackermann & Bishop, 2010). Recent efforts to produce the first gorilla Y‐chromosome assembly, despite the Y‐chromosome's highly repetitive nature and degradation, should in the future enable time and cost‐effective sequencing of further individuals from high‐quality DNA and facilitate the identification of SNP panels with higher power for phylogenetic analyses (Cechova et al, 2020; Tomaszkiewicz et al, 2016).…”

Dynamic evolution of great ape Y chromosomes

“…PRJNA602326 ) ( 66 ). Multiple sequence alignments of great ape Y chromosomes and of great ape X and Y chromosomes are available at ScholarSphere, https://doi.org/10.26207/9han-5s18 ( 67 ). Code is available at GitHub, https://github.com/makovalab-psu/great-ape-Y-evolution .…”

The contribution of sex chromosome conflict to disrupted spermatogenesis in hybrid house mice

“…Ampliconic genes are a common feature of mammalian sex chromosomes, and they tend to be expressed specifically during spermatogenesis (Li et al 2013; Soh et al 2014; Skinner et al 2016; Lucotte et al 2018; Bellott et al 2017; Hughes et al 2020; reviewed in Larson et al 2018a). Although difficult to quantify, evolution of ampliconic gene families involved in spermatogenesis is arguably one of the most rapidly evolving components of mammalian genomes (Mueller et al 2013; Soh et al 2014; Lucotte et al 2018; Cechova et al 2020; Vegesna et al 2020). Intragenomic conflict among sex chromosome ampliconic genes has been proposed as a mechanism through which hybrid incompatibilities have evolved in at least three mammali-an groups (cats, Davis et al 2015; primates, Dutheil et al 2015; and mice, Larson et al 2018a; Kruger et al 2019).…”

“…In cats, loci associated with hybrid sterility tend to be in or near high copy number genes (Davis et al 2015). In great apes, sex chromosome amplicon copy number can evolve rapidly (Lucotte et al 2018; Cechova et al 2020), and ampliconic regions on the X chromosome are thought to have experienced selective sweeps as a result of strong selection pressures imposed by intragenomic conflict with the Y chromosome (Nam et al 2015). These regions also overlap sections of the modern human X chromosome that lack Neandertal introgression, and therefore may represent regions involved in genetic incompatibilities between modern humans and Neandertals (Dutheil et al 2015).…”