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Reversal of an ancient sex chromosome to an autosome in Drosophila

Abstract

Although transitions of sex-determination mechanisms are frequent in species with homomorphic sex chromosomes1,2,3, heteromorphic sex chromosomes are thought to represent a terminal evolutionary stage owing to chromosome-specific adaptations such as dosage compensation or an accumulation of sex-specific mutations1,4. Here we show that an autosome of Drosophila, the dot chromosome, was ancestrally a differentiated X chromosome. We analyse the whole genome of true fruitflies (Tephritidae), flesh flies (Sarcophagidae) and soldier flies (Stratiomyidae) to show that genes located on the dot chromosome of Drosophila are X-linked in outgroup species, whereas Drosophila X-linked genes are autosomal. We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae. Our results reveal several puzzling aspects of Drosophila dot chromosome biology to be possible remnants of its former life as a sex chromosome, such as its minor feminizing role in sex determination5 or its targeting by a chromosome-specific regulatory mechanism6. We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome. Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

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Figure 1: Sex chromosomes in higher Diptera revealed by genome analysis.
Figure 2: Properties of the dot chromosome in Drosophila melanogaster that resemble that of an X chromosome.
Figure 3: Gene expression in early embryos and adult gonads in outgroup Diptera species.
Figure 4: Turnover of sex chromosomes in Drosophila.

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Acknowledgements

We thank S. Kunhi Purayil, I. Kadow, P. Mavragani, J. Larsson and U. Schmidt-Ott for samples, C. Zonneveld, L. Mazzon, D. Obbard, V. Aguiar, N. Gompel and J. Larsson for images, and Q. Zhou and Z. Walton for technical assistance. Funded by National Institutes of Health grants (R01GM076007 and R01GM093182) and a Packard Fellowship to D.B.

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B.V. and D.B. designed and performed the study, and wrote the manuscript.

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Correspondence to Doris Bachtrog.

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The authors declare no competing financial interests.

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All the DNA/RNA-sequencing reads generated in this study are deposited in the NCBI Short Reads Archive (http://www.ncbi.nlm.nih.gov/sra) under bioprojects SRP021043, SRP021044 and SRP021047.

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Vicoso, B., Bachtrog, D. Reversal of an ancient sex chromosome to an autosome in Drosophila . Nature 499, 332–335 (2013). https://doi.org/10.1038/nature12235

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