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.

Keywords: gene content evolution; palindromes; sex chromosomes.

Fig. 1.

Phylogenetic tree of nucleotide sequences. (A) Y chromosome. (B) Autosomes. Branch lengths (substitutions per 100 sites) were estimated from multispecies alignment blocks including all five species.

Fig. 2.

Evolution of Y chromosome gene content in great apes. The reconstructed history of gene birth and death for X-degenerate (blue) and ampliconic (red) genes was overlaid on the great ape phylogenetic tree (not drawn to scale), using macaque as an outgroup. The rates of gene birth and death (in events per million years) are shown in parentheses (for complete data, see SI Appendix, Fig. S6 and Table S4). The list at the root includes the genes that were present in the common ancestor of great apes and macaque. In addition to most of the genes on the human Y, the macaque Y harbors the X-degenerate MXRA5Y gene, which we found to be deleted in orangutan and pseudogenized in bonobo, chimpanzee, gorilla, and human. We currently cannot find a full-length copy of the VCY gene in bonobo (SI Appendix, Supplemental Note S7). TXLNGY and DDX3Y are also known as CYorf15B and DBY, respectively.

Fig. 3.

Evolution of sequences homologous to human and chimpanzee palindromes. (A) Heatmaps showing coverage for each palindrome in each species in the multispecies alignment (the last column includes all palindromes) and box plots representing copy number (natural log) of 1-kb windows which have homology with human or chimpanzee palindromes (the last box plot is for X-degenerate genes; the data for human and chimpanzee can be found in SI Appendix, Table S7). (B) The great ape phylogenetic tree (not drawn to scale) with evolution of human (shown in blue) and chimpanzee (red) palindromic sequences overlayed on it. Palindrome names in boldface indicate that their sequences were present in two or more copies. Negative (-) and positive (+) signs indicate loss and gain of palindrome sequence (possibly only partial), respectively. Arrows represent gain (↑) or loss (↓) of palindrome copy number. If several equally parsimonious scenarios were possible, we conservatively assumed a later date of acquisition of the multicopy state for a palindrome (SI Appendix, Supplemental Note S5, for additional details; the data are shown in SI Appendix, Table S7).

Fig. 4.

Chromatin contacts on the human and chimpanzee Y chromosomes, as evaluated from iPSCs. (A) Human Y chromosome contacts with palindromes (highlighted in light blue), pseudoautosomal regions (green), and centromere (red). The schematic representation of the sequencing classes on the Y chromosome is adapted from ref. . (B) Chimpanzee Y chromosome contacts with palindromes (highlighted in light blue). The schematic representation of the sequencing classes on the Y chromosome is adapted from ref. . (C) Chromatin interactions for the three largest palindromes on the human Y (the next three largest palindromes are displayed in SI Appendix, Fig. S10). To resolve ambiguity due to multimapping reads, each interaction was assigned a probability based on the fraction of reads supporting it (see SI Appendix, Supplemental Methods, for details). Palindrome arms are shown as blue arrows, and the spacer is shown as white space between them.