Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content

Abstract

With the sequencing of the male-specific region of the chimpanzee Y chromosome, it is now possible to make comparisons with the human Y sequence and to learn more about the recent evolution of the human Y chromosome. The two sequences differ markedly in structure and gene content, indicating rapid evolution during the past 6 million years. This finding is at odds with the common view that Y chromosomes are essentially static structures that evolve only very slowly by genetic loss. Rather, renovation and remodelling dominate the evolution of human and chimpanzee Y chromosomes. Possible reasons for this extraordinary divergence include genetic hitchhiking effects, species-specific mating behaviours and the Y chromosome's role in sperm production. Little is known about the recent evolution of the Y chromosome because only the human Y chromosome has been fully sequenced. The sequencing of the male-specific region of the Y chromosome (MSY) in the chimpanzee and comparison between the MSYs of the two species now reveals that they differ radically in sequence structure and gene content, indicating rapid evolution over the past 6 million years. The human Y chromosome began to evolve from an autosome hundreds of millions of years ago, acquiring a sex-determining function and undergoing a series of inversions that suppressed crossing over with the X chromosome1,2. Little is known about the recent evolution of the Y chromosome because only the human Y chromosome has been fully sequenced. Prevailing theories hold that Y chromosomes evolve by gene loss, the pace of which slows over time, eventually leading to a paucity of genes, and stasis3,4. These theories have been buttressed by partial sequence data from newly emergent plant and animal Y chromosomes5,6,7,8, but they have not been tested in older, highly evolved Y chromosomes such as that of humans. Here we finished sequencing of the male-specific region of the Y chromosome (MSY) in our closest living relative, the chimpanzee, achieving levels of accuracy and completion previously reached for the human MSY. By comparing the MSYs of the two species we show that they differ radically in sequence structure and gene content, indicating rapid evolution during the past 6 million years. The chimpanzee MSY contains twice as many massive palindromes as the human MSY, yet it has lost large fractions of the MSY protein-coding genes and gene families present in the last common ancestor. We suggest that the extraordinary divergence of the chimpanzee and human MSYs was driven by four synergistic factors: the prominent role of the MSY in sperm production, ‘genetic hitchhiking’ effects in the absence of meiotic crossing over, frequent ectopic recombination within the MSY, and species differences in mating behaviour. Although genetic decay may be the principal dynamic in the evolution of newly emergent Y chromosomes, wholesale renovation is the paramount theme in the continuing evolution of chimpanzee, human and perhaps other older MSYs.