Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog Glandirana rugosa

Genes (Basel). 2023 Jan 18;14(2):257. doi: 10.3390/genes14020257.

Abstract

Genetic sex-determination features male (XX/XY) or female heterogamety (ZZ/ZW). To identify similarities and differences in the molecular evolution of sex-linked genes between these systems, we directly compared the sex chromosome systems existing in the frog Glandirana rugosa. The heteromorphic X/Y and Z/W sex chromosomes were derived from chromosomes 7 (2n = 26). RNA-Seq, de novo assembly, and BLASTP analyses identified 766 sex-linked genes. These genes were classified into three different clusters (XW/YZ, XY/ZW, and XZ/YW) based on sequence identities between the chromosomes, probably reflecting each step of the sex chromosome evolutionary history. The nucleotide substitution per site was significantly higher in the Y- and Z-genes than in the X- and W- genes, indicating male-driven mutation. The ratio of nonsynonymous to synonymous nucleotide substitution rates was higher in the X- and W-genes than in the Y- and Z-genes, with a female bias. Allelic expression in gonad, brain, and muscle was significantly higher in the Y- and W-genes than in the X- and Z-genes, favoring heterogametic sex. The same set of sex-linked genes showed parallel evolution across the two distinct systems. In contrast, the unique genomic region of the sex chromosomes demonstrated a difference between the two systems, with even and extremely high expression ratios of W/Z and Y/X, respectively.

Keywords: dN/dS ratio; gene expression; heterogametic sex; male-biased mutation.

MeSH terms

  • Animals
  • Anura / genetics
  • Evolution, Molecular
  • Female
  • Male
  • Nucleotides
  • Ranidae* / genetics
  • Sex Chromosomes*

Substances

  • Nucleotides

Grants and funding

This research received no external funding.