Abstract
Sex-chromosomes have formed repeatedly across Diptera from ordinary autosomes, and X-chromosomes mostly conserve their ancestral genes. Y-chromosomes are characterized by abundant gene-loss and an accumulation of repetitive DNA, yet the nature of the gene repertoire of fly Y-chromosomes is largely unknown. Here we trace gene-content evolution of Y-chromosomes across 22 Diptera species, using a subtraction pipeline that infers Y genes from male and female genome, and transcriptome data. Few genes remain on old Y-chromosomes, but the number of inferred Y-genes varies substantially between species. Young Y-chromosomes still show clear evidence of their autosomal origins, but most genes on old Y-chromosomes are not simply remnants of genes originally present on the proto-sex-chromosome that escaped degeneration, but instead were recruited secondarily from autosomes. Despite almost no overlap in Y-linked gene content in different species with independently formed sex-chromosomes, we find that Y-linked genes have evolved convergent gene functions associated with testis expression. Thus, male-specific selection appears as a dominant force shaping gene-content evolution of Y-chromosomes across fly species.
Highlights
Sex-chromosomes have formed repeatedly across Diptera from ordinary autosomes, and X-chromosomes mostly conserve their ancestral genes
Our initial application of these approaches to our male and female genomic fly data was of limited success to reliably identify Y genes[9], presumably due to a combination of factors: Y chromosomes have few genes and mainly consist of repetitive DNA, and our genome assemblies for the various fly taxa from next-generation sequencing data are more fragmented than the well-curated Drosophila or Anopheles genomes, and especially so at repeat-rich regions
D. pseudobscura genome, we identify 63 transcripts that are highly similar to the reference genome sequence ( > 95% of nucleotides mapping over 50% of the transcript); 20 of these transcripts map to unplaced, 39 transcripts are located on Muller element C, which is the homolog of the recently formed neo-sex chromosomes in D. miranda, and only 4 map to other genomic locations
Summary
Sex-chromosomes have formed repeatedly across Diptera from ordinary autosomes, and X-chromosomes mostly conserve their ancestral genes. We trace gene-content evolution of Y-chromosomes across 22 Diptera species, using a subtraction pipeline that infers Y genes from male and female genome, and transcriptome data. Sex chromosomes are derived from ordinary autosomes, yet old X and Y chromosomes contain a vastly different gene repertoire. We recently showed that superficially similar karyotypes conceal the true extent of sex chromosome variation in Diptera: whole-genome analysis in 37 fly species belonging to 22 families identified over a dozen different sex chromosome configurations in flies based on gene content conservation of the X chromosome[9]. Several Y-linked proteincoding genes in Drosophila melanogaster, for example, carry mega-base sized introns consisting of repetitive transposable element (TE) and satellite-derived DNA11, making it impossible to assemble them using next-generation sequencing approaches[12, 13] (though the application of long-read PacBio. Discard transcripts (≤60% coverage in males and >10% coverage in females, for reads with ≤2 mismatches)
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