Sex chromosome evolution: molecular aspects of Y-chromosome degeneration in Drosophila

Abstract

Ancient Y-chromosomes of various organisms contain few active genes and an abundance of repetitive DNA. The neo-Y chromosome of Drosophila miranda is in transition from an ordinary autosome to a genetically inert Y-chromosome, while its homolog, the neo-X chromosome, is evolving partial dosage compensation. Here, I compare four large genomic regions located on the neo-sex chromosomes that contain a total of 12 homologous genes. In addition, I investigate the partial coding sequence for 56 more homologous gene pairs from the neo-sex chromosomes. Little modification has occurred on the neo-X chromosome, and genes are highly constrained at the protein level. In contrast, a diverse array of molecular changes is contributing to the observed degeneration of the neo-Y chromosome. In particular, the four large regions surveyed on the neo-Y chromosome harbor several transposable element insertions, large deletions, and a large structural rearrangement. About one-third of all neo-Y-linked genes are nonfunctional, containing either premature stop codons and/or frameshift mutations. Intact genes on the neo-Y are accumulating amino acid and unpreferred codon changes. In addition, both 5'- and 3'-flanking regions of genes and intron sequences are less constrained on the neo-Y relative to the neo-X. Despite heterogeneity in levels of dosage compensation along the neo-X chromosome of D. miranda, the neo-Y chromosome shows surprisingly uniform signs of degeneration.

Figure 1.

Schematic karyotype of the D. miranda neo-sex chromosomes. The neo-sex chromosomes were formed by the fusion of an autosome (Chromosome 3 of D. pseudoobscura) to the Y-chromosome of D. miranda. Shown are the relative locations of the four genomic regions investigated on the neo-X chromosome of D. miranda.

Figure 2.

Organization of the four genomic regions investigated on the neo-sex chromosomes. (A) The exu1 region (Bachtrog 2003a). A total of ∼40 kb of neo-X and ∼45 kb of neo-Y sequence was investigated. (B) The mle genomic region. Here 8 kb of neo-X- and 25 kb of neo-Y-derived sequence were analyzed. (C) The robo genomic region. A total of 6 kb of neo-X and 11 kb of neo-Y sequence was analyzed. (D) The dpn genomic region. Here 24 kb was analyzed from the neo-X chromosome, and 17 kb from the neo-Y. Protein-coding genes are shown as gray bars, and transposable element insertions are displayed as red bars. Amino acid changes are indicated as gray triangles, premature stop codons are displayed as red triangles, and deletions destroying the reading frame of the protein are represented as blue bars.

Figure 3.

Insertion site of the ohura transposable element on the neo-Y chromosome of D. miranda. The TE insertion is flanked by a 5-bp target site duplication. The ohura TE is flanked by a 267-bp LTR, and contains three protein domains, a protease (PR), an intergrase (IN), and a reverse transcriptase (RT).

Figure 4.

Evolution of protein-coding genes on the neo-sex chromosomes. Boxes correspond to exons (with left or right arrows corresponding to the first or last exon of a gene, respectively), and lines correspond to introns or flanking intergenic regions. Gray triangles indicate amino acid changes, blue bars represent frameshift deletions, and red triangles correspond to premature stop codons.