Shared evolutionary trajectories of three independent neo-sex chromosomes in Drosophila
- Masafumi Nozawa1,2,
- Yohei Minakuchi3,
- Kazuhiro Satomura1,5,
- Shu Kondo4,6,
- Atsushi Toyoda3 and
- Koichiro Tamura1,2
- 1Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan;
- 2Research Center for Genomics and Bioinformatics, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan;
- 3Comparative Genomics Laboratory, Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan;
- 4Invertebrate Genetics Laboratory, Department of Chromosome Science, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan
Abstract
Dosage compensation (DC) on the X Chromosome counteracts the deleterious effects of gene loss on the Y Chromosome. However, DC is not efficient if the X Chromosome also degenerates. This indeed occurs in Drosophila miranda, in which both the neo-Y and the neo-X are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that emerged independently in D. albomicans and D. americana and reanalyzed neo-sex chromosome evolution in D. miranda. Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on the neo-X is also accelerated in D. albomicans and D. americana although to a lesser extent than in D. miranda. In males, neo-X-linked genes whose neo-Y-linked homologs are pseudogenized tended to be up-regulated more than those whose neo-Y-linked homologs remain functional. Moreover, genes under strong functional constraint and genes highly expressed in the testis tended to remain functional on the neo-X and neo-Y, respectively. Focusing on the D. miranda and D. albomicans neo-sex chromosomes that emerged independently from the same autosome, we further found that the same genes tend to become pseudogenized in parallel on the neo-Y. These genes include Idgf6 and JhI-26, which may be unnecessary or even harmful in males. Our results indicate that neo-sex chromosomes in Drosophila share a common evolutionary trajectory after their emergence, which may prevent sex chromosomes from being an evolutionary dead end.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.275503.121.
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Freely available online through the Genome Research Open Access option.
- Received March 11, 2021.
- Accepted July 22, 2021.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
