Sex-specific adaptation drives early sex chromosome evolution in Drosophila

Abstract

Most species' sex chromosomes are derived from ancient autosomes and show few signatures of their origins. We studied the sex chromosomes of Drosophila miranda, where a neo-Y chromosome originated only approximately 1 million years ago. Whole-genome and transcriptome analysis reveals massive degeneration of the neo-Y, that male-beneficial genes on the neo-Y are more likely to undergo accelerated protein evolution, and that neo-Y genes evolve biased expression toward male-specific tissues--the shrinking gene content of the neo-Y becomes masculinized. In contrast, although older X chromosomes show a paucity of genes expressed in male tissues, neo-X genes highly expressed in male-specific tissues undergo increased rates of protein evolution if haploid in males. Thus, the response to sex-specific selection can shift at different stages of X differentiation, resulting in masculinization or demasculinization of the X-chromosomal gene content.

Figure 1

(A) The reconstructed evolutionary history of D. miranda sex chromosomes. The ancestral sex chromosome chrXL (red) fused to Muller-D element, creating chrXR (green) and the unfused element became part of the heterochromatic ancestral chrY (black). In D. miranda, Muller-C subsequently fused to chrY, creating a neo-Y chromosome (fused Muller-C element, dark brown), and a neo-X (unfused Muller-C element, light brown). (B) Shown are coverage (mapped read counts every 50kb region) and SNP density (sites/kb) derived separately from male and female genomic reads in a 5kb sliding window across the D. miranda genome. The high male SNP density along the neo-X (male: 3.696 vs. female: 0.080 sites/kb) reflects divergence between the neo-X and neo-Y chromosome.

Figure 2

(A) Composition of neo-Y genes with regards to inferred functionality (green: intact ORFs and detectable expression in adult male; grey: disrupted ORF and/or silenced expression; yellow: genes without neo-X expression or without diagnostic SNPs). (B) The chromosomal distribution of non-functional genes across a sliding window size of 20 genes (black line). Average neo-X expression bias within the investigated window was calculated from log ratios of neo-X vs. neo-Y expression for functional (green) and non-functional (grey) genes. Functional neo-Y genes show significantly less neo-X biased expression than non-functional genes (boxplot, P<2.2e^-16, Wilcoxon test). (C) Evolutionary rate comparisons (K_a/K_s ratios relative to D. pseudoobscura) among genes on different chromosomes. Wilcoxon tests show significant differences in K_a/K_s ratios between neo-X vs. neo-Y genes, genes with intact neo-Y copies with vs. without expression (P=0.000242) and disrupted vs. intact transcribed neo-Y genes (P=2.971e^-12). Different levels of significance are marked as asterisks. (D) The frequency distribution of K_a/K_s ratios of neo-X and neo-Y genes.

Figure 3

(A) Sex-specific fitness effects and sexual antagonism of neo-sex genes (light-blue: male-fitness related; light-red: female-fitness related; dark-blue: male-beneficial/female-detrimental; dark-red: female-beneficial/male-detrimental). Significance is evaluated by comparing all neo-sex genes to either fast evolving or non-functional neo-Y genes (‘*’ P-value <0.05, ‘**’ P-value <0.01). (B) The number of neo-X biased (red), neo-Y biased (blue) and non-biased (green) genes in different tissues of male D. miranda.

Figure 4

(A) The observed/expected ratio of genes highly expressed (top 500; for different cutoffs see fig. S7) in testis or accessory glands. (B) Log-based absolute expression levels (FPKM) from ovary for each chromosome (see also fig. S7). (C) The ω ratio on the neo-X branch at hemizygous and diploid neo-X genes.