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 share 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, which includes chimpanzee and bonobo, experienced accelerated substitution rates. 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 multicopy 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. Our results highlight the dynamic mode of Y chromosome evolution and open avenues for studies of male-specific dispersal in endangered great ape species.

A near complete genome for goat genetic and genomic research

“…We observed higher substitution rates for the Y chromosome than for autosomes across the four lineages, suggesting that the Caprini and Bovini species are subjected to male-driven molecular evolution [ 82 ]. This male mutation bias has also been observed in other mammalian species, including primates and rodents [ 83 ], which could be attributed to the relative excess of cell divisions in the male germline compared with the female germline [ 75 ]. We also found a similar substitution rate for the Y chromosome of goat and sheep which shared a common ancestor 5.85 million years ago, implying that the evolution rates in Caprini species are similar.…”

New insights into the evolution of human Y chromosome palindromes through mutation and gene conversion

“…Although the relevance of gene conversion in the evolution of palindromes has been profoundly recognized ( 1 , 3 , 6 , 14 , 21 , 22 , 42 , 43 ), the dynamic of this mechanism is still nuanced. More generally, the evolutionary dynamics of palindromic structures (arms and spacer) and the reason for their ubiquitous existence on sex haploid chromosomes have not been fully clarified yet.…”

“…A similar result has been previously observed by ( 41 ) which reported P6 as the only human palindrome showing the conservation of two arms in more than 1200 Y chromosomes belonging to several different haplogroups. Moreover, among human palindromes, P6 is the element exhibiting the strongest evolutionary conservation, with a sequence coverage ranging from ~89 to ~ 96% of other great ape Y assemblies ( 43 ). Indeed, despite the absence of protein-coding genes in this palindrome, evidence of elements regulating gene expression overlapping P6 arms have been recently reported ( 43 ).…”

“…Moreover, among human palindromes, P6 is the element exhibiting the strongest evolutionary conservation, with a sequence coverage ranging from ~89 to ~ 96% of other great ape Y assemblies ( 43 ). Indeed, despite the absence of protein-coding genes in this palindrome, evidence of elements regulating gene expression overlapping P6 arms have been recently reported ( 43 ). Therefore, the high conservation and the presence of functional sequences may suggest a possible strong action of natural selection in the evolution of this element.…”

Probably Correct: Rescuing Repeats with Short and Long Reads

“…Ampliconic regions host large inverted repeats, i.e., palindromes, which are then omitted from traditional pipelines. Using a probabilistic approach implemented in the package mHi-C [ 61 ], Cechova, Vegesna, and colleagues were able to analyze palindromic arms of human palindromes and found a higher density of chromatin interactions; none of these regions could be analyzed if multi-mapping reads had been excluded [ 62 ].…”