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. 2009 Jul;5(7):e1000568.
doi: 10.1371/journal.pgen.1000568. Epub 2009 Jul 17.

Evolution and survival on eutherian sex chromosomes

Melissa A Wilson  1 , Kateryna D Makova
Affiliations

Evolution and survival on eutherian sex chromosomes

Melissa A Wilson et al. PLoS Genet. 2009 Jul.

Abstract

Since the two eutherian sex chromosomes diverged from an ancestral autosomal pair, the X has remained relatively gene-rich, while the Y has lost most of its genes through the accumulation of deleterious mutations in nonrecombining regions. Presently, it is unclear what is distinctive about genes that remain on the Y chromosome, when the sex chromosomes acquired their unique evolutionary rates, and whether X-Y gene divergence paralleled that of paralogs located on autosomes. To tackle these questions, here we juxtaposed the evolution of X and Y homologous genes (gametologs) in eutherian mammals with their autosomal orthologs in marsupial and monotreme mammals. We discovered that genes on the X and Y acquired distinct evolutionary rates immediately following the suppression of recombination between the two sex chromosomes. The Y-linked genes evolved at higher rates, while the X-linked genes maintained the lower evolutionary rates of the ancestral autosomal genes. These distinct rates have been maintained throughout the evolution of X and Y. Specifically, in humans, most X gametologs and, curiously, also most Y gametologs evolved under stronger purifying selection than similarly aged autosomal paralogs. Finally, after evaluating the current experimental data from the literature, we concluded that unique mRNA/protein expression patterns and functions acquired by Y (versus X) gametologs likely contributed to their retention. Our results also suggest that either the boundary between sex chromosome strata 3 and 4 should be shifted or that stratum 3 should be divided into two strata.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic analysis and branch length comparisons for concatenated gene sequences: gene-by-gene (upper panel) and exon-by-exon (lower panel) analysis.
Xpter and Xqter—the termini of the short and long arms of the X chromosome, respectively. Red and blue boxes indicate the post- and pre-radiation topology, respectively, and white boxes represent masked out sequence (see Materials and Methods).
Figure 2
Figure 2. Pre-radiation phylogeny and evolutionary rate comparisons.
(A) Phylogeny for the pre-radiation topology. Exons with less than 50% bootstrap support for clades with either the pre- or post-radiation topology, fewer than 24 nucleotides aligned across all species, or inconsistent with the topology of the whole gene were excluded. Branch lengths are proportional to the estimated synonymous substitutions per site, and are labeled with the nonsynonymous-to-synonymous rate ratios (KA/KS). (B) Branch length comparisons for the pre-radiation topology. We present the model-averaged probabilities (not P values) that two branches have the same Ka/Ks ratio, and so corrections for multiple tests are neither needed nor appropriate (see Materials and Methods). Significant values are shown in bold.
Figure 3
Figure 3. Post-radiation phylogeny and evolutionary rate comparisons.
(A) Phylogeny for the post-radiation topology. Exons with less than 50% bootstrap support for clades with either the pre- or post-radiation topology, fewer than 24 nucleotides aligned across all species, or inconsistent with the topology of the whole gene were excluded. Branch lengths are proportional to the estimated synonymous substitutions per site, and are labeled with the nonsynonymous-to-synonymous rate ratios (KA/KS). (B) Branch length comparisons for the post-radiation topology. We present the model-averaged probabilities (not P values) that two branches have the same Ka/Ks ratio, and so corrections for multiple tests are neither needed nor appropriate (see Materials and Methods). Significant values are shown in bold.
Figure 4
Figure 4. New stratum boundary.
The previous descriptions of the stratum3–stratum4 boundary are shown, along with a new boundary region, identified by this study.
Figure 5
Figure 5. Tissue-specific divergence between human X and Y gametologs.
We compared divergence in gene expression based on the presence or absence of gametolog expression and, when both gametologs in a pair were expressed, used the fold change to compare the expression levels between the two gametologs in each pair (see Materials and Methods). Blue field indicates tissues in which the Y gametolog is expressed at a higher level than the X gametolog; green field indicates tissues in which the X gametolog is expressed at a higher level than the Y gametolog; white field with a value indicates similar (less than 25% different) expression for X and Y; and an empty white field indicates that neither gametolog is expressed in a particular tissue. Numbers represent log2(X/Y), where X and Y are X and Y expression values, respectively. Labels “X” or ”Y” indicate that only the X or only the Y gametolog is expressed. The data for all 11 gametologous pairs present on the array from a study by Su and colleagues are shown (TMSB4X/Y pair was not present on the array).
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