General gene movement off the X chromosome in the Drosophila genus.

In Drosophila melanogaster, there is an excess of genes duplicated by retroposition from the X chromosome to the autosomes. Most of those retrogenes that originated on the X chromosome have testis expression pattern. These observations could be explained by natural selection favoring genes that avoided spermatogenesis X inactivation or by sexual antagonistic effects favoring the fixation of male beneficial mutations on the autosomes. If natural selection played the essential role in distributing male-related genes, then the out-of-the-X chromosomal gene movement should not be limited to retrogenes. Here, we studied DNA-based interchromosome gene movement patterns by analyzing relocated genes that were previously identified in 12 Drosophila genome sequences. We found a significant excess of gene movement out of the X chromosome. In addition, we were able to extend previous retrogene movement analysis to species and branches other than those involving D. melanogaster, confirming the pervasiveness of gene movement out of the X chromosome. Also, for X chromosome-to-autosome (X-->A) movement, we observed high testis expression of relocated genes as opposed to the low testis expression of parental genes, corroborating the involvement of the male germ line on the gene movement process. These analyses of both DNA-based and RNA-based gene relocations reveal that the out-of-the-X movement of testis-expressed genes is a general pattern in the Drosophila genus.