Carvalho, Antonio; Vicoso, BeatrizIST Austria ; Russo, Claudia; Swenor, Bonnielin; Clark, Andrew
Contrary to the pattern seen in mammalian sex chromosomes, where most Y-linked genes have X-linked homologs, the Drosophila X and Y chromosomes appear to be unrelated. Most of the Y-linked genes have autosomal paralogs, so autosome-to-Y transposition must be the main source of Drosophila Y-linked genes. Here we show how these genes were acquired. We found a previously unidentified gene (flagrante delicto Y, FDY) that originated from a recent duplication of the autosomal gene vig2 to the Y chromosome of Drosophila melanogaster. Four contiguous genes were duplicated along with vig2, but they became pseudogenes through the accumulation of deletions and transposable element insertions, whereas FDY remained functional, acquired testis-specific expression, and now accounts for ∼20% of the vig2-like mRNA in testis. FDY is absent in the closest relatives of D. melanogaster, and DNA sequence divergence indicates that the duplication to the Y chromosome occurred ∼2 million years ago. Thus, FDY provides a snapshot of the early stages of the establishment of a Y-linked gene and demonstrates how the Drosophila Y has been accumulating autosomal genes.
This work was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), FAPERJ, and CAPES (to A.B.C.), and National Institutes of Health Grant R01 GM64590 (to A.G.C. and A.B.C.). We thank M. Vibranovski, C. Bergman, and the Berkeley Drosophila Genome Project for access to unpublished data; M. Vibranovski, R. Hoskins, S. Celniker, C. Kennedy, J. Carlson, S. Galasinski, B. Wakimoto, J. Yasuhara, G. Sutton, M. Kuhner, J. Felsenstein, and C. Santos for help in various steps of the work; and B. Bitner-Mathe, R. Ventura, the members of the A.B.C. and A.G.C. laboratories, and two reviewers for many valuable comments on the manuscript.
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Carvalho A, Vicoso B, Russo C, Swenor B, Clark A. Birth of a new gene on the Y chromosome of Drosophila melanogaster. PNAS. 2015;112(40):12450-12455. doi:10.1073/pnas.1516543112
Carvalho, A., Vicoso, B., Russo, C., Swenor, B., & Clark, A. (2015). Birth of a new gene on the Y chromosome of Drosophila melanogaster. PNAS, 112(40), 12450–12455. https://doi.org/10.1073/pnas.1516543112
Carvalho, Antonio, Beatriz Vicoso, Claudia Russo, Bonnielin Swenor, and Andrew Clark. “Birth of a New Gene on the Y Chromosome of Drosophila Melanogaster.” PNAS 112, no. 40 (2015): 12450–55. https://doi.org/10.1073/pnas.1516543112.
A. Carvalho, B. Vicoso, C. Russo, B. Swenor, and A. Clark, “Birth of a new gene on the Y chromosome of Drosophila melanogaster,” PNAS, vol. 112, no. 40, pp. 12450–12455, 2015.
Carvalho A, Vicoso B, Russo C, Swenor B, Clark A. 2015. Birth of a new gene on the Y chromosome of Drosophila melanogaster. PNAS. 112(40), 12450–12455.
Carvalho, Antonio, et al. “Birth of a New Gene on the Y Chromosome of Drosophila Melanogaster.” PNAS, vol. 112, no. 40, National Academy of Sciences, 2015, pp. 12450–55, doi:10.1073/pnas.1516543112.
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