A complex suite of forces drives gene traffic from Drosophila X chromosomes

Abstract

Theoretical studies predict X chromosomes and autosomes should be under different selection pressures, and there should therefore be differences in sex-specific and sexually antagonistic gene content between the X and the autosomes. Previous analyses have identified an excess of genes duplicated by retrotransposition from the X chromosome in Drosophila melanogaster. A number of hypotheses may explain this pattern, including mutational bias, escape from X-inactivation during spermatogenesis, and the movement of male-favored (sexually antagonistic) genes from a chromosome that is predominantly carried by females. To distinguish among these processes and to examine the generality of these patterns, we identified duplicated genes in nine sequenced Drosophila genomes. We find that, as in D. melanogaster, there is an excess of genes duplicated from the X chromosome across the genus Drosophila. This excess duplication is due almost completely to genes duplicated by retrotransposition, with little to no excess from the X among genes duplicated via DNA intermediates. The only exception to this pattern appears within the burst of duplication that followed the creation of the Drosophila pseudoobscura neo-X chromosome. Additionally, we examined genes relocated among chromosomal arms (i.e., genes duplicated to new locations coupled with the loss of the copy in the ancestral locus) and found an excess of genes relocated off the ancestral X and neo-X chromosomes. Interestingly, many of the same genes were duplicated or relocated from the independently derived neo-X chromosomes of D. pseudoobscura and Drosophila willistoni, suggesting that natural selection favors the traffic of genes from X chromosomes. Overall, we find that the forces driving gene duplication from X chromosomes are dependent on the lineage in question, the molecular mechanism of duplication considered, the preservation of the ancestral copy, and the age of the X chromosome.

Keywords: X-inactivation; gene duplication; neo-X chromosomes; retrotransposition; sex chromosomes.

FIG. 1.—

Phylogeny of some Drosophila species with sequenced genomes and their karyotypes. Lineages upon which duplicated and relocated genes were identified are highlighted in bold. Homologous chromosomes arms (Muller elements) are the same color for all species. X, X chromosome; A, autosome.

FIG. 2.—

Lineage-specific interarm duplications. Duplicated genes were identified using the phylogenetic method. Gray bars are the observed counts and black bars are the expected counts (based on chromosome sizes and hemizygosity). X, ancestral X chromosome; A, autosome; neo-X, neo-X chromosome. Arrows indicated direction of duplication event.

FIG. 3.—

Mechanisms of lineage-specific gene duplications. Observed counts of the number of DNA duplications (black), retroposed duplications (white), and ambiguous duplications (gray) are shown for interarm duplications between X chromosomes and autosomes. Duplicated genes were identified using the phylogenetic method, limited to two copies per lineage.

FIG. 4.—

Lineage-specific gene relocation between chromosome arms. The observed (gray) and expected (black) counts of relocated genes are shown for all possible directions of relocation. A, autosome; X, ancestral X chromosome; neo-X, neo-X chromosome.

FIG. 5.—

A burst of duplication followed the creation of the neo-X chromosome in Drosophila pseudoobscura. The number of paralogs with divergence between copies is graphed for three classes of duplicated genes in the D. pseudoobscura genome: autosome-to-autosome (large dashes, hollow diamonds), ancestral X-to-autosome (solid line, solid diamonds), and neo-X-to-autosome (small dashes, hollow squares). Duplicated genes were identified using the phylogenetic method.