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

Abstract

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 chromosome. 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 stasis. These theories have been buttressed by partial sequence data from newly emergent plant and animal Y chromosomes, 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.

Figure 1

Comparison of chimpanzee and human Y chromosomes. (a) Schematic representations of chromosomes. Yp, short arm. cen, centromere. Yq, long arm. For both chromosomes, male-specific region (MSY) is indicated. Six sequence classes are shown, four of which are MSY euchromatin. (“Other” denotes MSY single-copy sequences that are not X-degenerate or X-transposed.) Chromosomes drawn to scale with exception of large heterochromatic block on human Yq. (b) Sizes (in Mb) of four MSY euchromatin sequence classes in chimpanzee and human. (c) Percentages of ampliconic and X-degenerate sequences present on chimpanzee Y chromosome that are also present on human Y chromosome, and vice versa.

Figure 2

Dot plots of DNA sequence identity between chimpanzee and human Y chromosomes (at left) and chromosomes 21 (at right). Each dot represents 100% chimpanzee-human identity within a 200-bp window. In the Y-chromosome plot, the human chromosome is oriented with short arm to top and long arm to bottom, and the chimpanzee chromosome is oriented with short arm to left and long arm to right. For chromosome 21, which is acrocentric, the plot represents only the long arm.

Figure 3

Triangular dot plots of DNA sequence identities within euchromatic MSY of chimpanzee (top) and human (bottom). Each dot represents 100% intrachromosomal identity within a 200-bp window. Red dots represent matches between heterochromatic sequences. Direct repeats appear as horizontal lines, inverted repeats as vertical lines, and palindromes as vertical lines that nearly intersect the baseline. Insets indicate that each large triangular plot contains two smaller triangles (one revealing sequence identities within Yp and one revealing identities within Yq) and a rectangle (revealing sequence identities between Yp and Yq). Immediately below plots are schematic representations of chromosomes. Triangles below chromosome schematics denote sizes and locations of palindromes. Gaps between opposed triangles represent the non-duplicated spacers between palindrome arms.