Where Are the Formerly Y-linked Genes in the Ryukyu Spiny Rat that has Lost its Y Chromosome?

Abstract

It has been predicted that the highly degenerate mammalian Y chromosome will be lost eventually. Indeed, Y was lost in the Ryukyu spiny rat Tokudaia osimensis, but the fate of the formerly Y-linked genes is not completely known. We looked for all 12 ancestrally Y-linked genes in a draft T. osimensis genome sequence. Zfy1, Zfy2, Kdm5d, Eif2s3y, Usp9y, Uty, and Ddx3y are putatively functional and are now located on the X chromosome, whereas Rbmy, Uba1y, Ssty1, Ssty2, and Sry are missing or pseudogenized. Tissue expressions of the mouse orthologs of the retained genes are significantly broader/higher than those of the lost genes, suggesting that the destinies of the formerly Y-linked genes are related to their original expressions. Interestingly, patterns of gene retention/loss are significantly more similar than by chance across four rodent lineages where Y has been independently lost, indicating a level of certainty in the fate of Y-linked genes even when the chromosome is gone.

Keywords: Tokudaia osimensis; Y chromosome; evolution; gene expression; gene loss; spiny rat.

Fig. 1.

Mouse tissue expressions of 12 ancestrally Y-linked genes. a) Box plots of mean expression scores across tissues for the mouse orthologs of T. osimensis retained and lost formerly Y-linked genes, respectively. The lower and upper edges of a box represent the first and third quartiles, respectively, the horizontal line inside the box indicates the median, the whiskers extend to the most extreme values inside inner fences (median ± 1.5× interquartile range) and the dots show outliers. P-values are based on two-sample, two-tailed t-tests with unequal variances. b) Heatmap of expression scores in 34 tissues. Mouse orthologs of the genes that are lost or pseudogenized in T. osimensis are color-coded in red, whereas those of the retained genes are in black. The dendrogram produced by hierarchical clustering is shown on the leftmost of the heatmap.