Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
- Guang-An Lu1,
- Yixin Zhao1,
- Hao Yang1,
- Ao Lan1,
- Suhua Shi1,
- Zhongqi Liufu1,
- Yumei Huang1,
- Tian Tang1,
- Jin Xu1,2,
- Xu Shen1 and
- Chung-I Wu1,3
- 1State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, Guangdong, China;
- 2Center for Personal Dynamic Regulomes, Stanford University, Stanford, California 94305, USA;
- 3Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA
Abstract
The prevalence of de novo coding genes is controversial due to length and coding constraints. Noncoding genes, especially small ones, are freer to evolve de novo by comparison. The best examples are microRNAs (miRNAs), a large class of regulatory molecules ∼22 nt in length. Here, we study six de novo miRNAs in Drosophila, which, like most new genes, are testis-specific. We ask how and why de novo genes die because gene death must be sufficiently frequent to balance the many new births. By knocking out each miRNA gene, we analyzed their contributions to the nine components of male fitness (sperm production, length, and competitiveness, among others). To our surprise, the knockout mutants often perform better than the wild type in some components, and slightly worse in others. When two of the younger miRNAs are assayed in long-term laboratory populations, their total fitness contributions are found to be essentially zero. These results collectively suggest that adaptive de novo genes die regularly, not due to the loss of functionality, but due to the canceling out of positive and negative fitness effects, which may be characterized as “quasi-neutrality.” Since de novo genes often emerge adaptively and become lost later, they reveal ongoing period-specific adaptations, reminiscent of the “Red-Queen” metaphor for long-term evolution.
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 http://www.genome.org/cgi/doi/10.1101/gr.233809.117.
- Received December 19, 2017.
- Accepted July 20, 2018.
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