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Death of new microRNA genes in Drosophila via gradual loss of fitness advantages

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 nov...

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Autores principales: Lu, Guang-An, Zhao, Yixin, Yang, Hao, Lan, Ao, Shi, Suhua, Liufu, Zhongqi, Huang, Yumei, Tang, Tian, Xu, Jin, Shen, Xu, Wu, Chung-I
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6120634/
https://www.ncbi.nlm.nih.gov/pubmed/30049791
http://dx.doi.org/10.1101/gr.233809.117
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author Lu, Guang-An
Zhao, Yixin
Yang, Hao
Lan, Ao
Shi, Suhua
Liufu, Zhongqi
Huang, Yumei
Tang, Tian
Xu, Jin
Shen, Xu
Wu, Chung-I
author_facet Lu, Guang-An
Zhao, Yixin
Yang, Hao
Lan, Ao
Shi, Suhua
Liufu, Zhongqi
Huang, Yumei
Tang, Tian
Xu, Jin
Shen, Xu
Wu, Chung-I
author_sort Lu, Guang-An
collection PubMed
description 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.
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spelling pubmed-61206342019-03-01 Death of new microRNA genes in Drosophila via gradual loss of fitness advantages Lu, Guang-An Zhao, Yixin Yang, Hao Lan, Ao Shi, Suhua Liufu, Zhongqi Huang, Yumei Tang, Tian Xu, Jin Shen, Xu Wu, Chung-I Genome Res Research 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. Cold Spring Harbor Laboratory Press 2018-09 /pmc/articles/PMC6120634/ /pubmed/30049791 http://dx.doi.org/10.1101/gr.233809.117 Text en © 2018 Lu et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Lu, Guang-An
Zhao, Yixin
Yang, Hao
Lan, Ao
Shi, Suhua
Liufu, Zhongqi
Huang, Yumei
Tang, Tian
Xu, Jin
Shen, Xu
Wu, Chung-I
Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title_full Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title_fullStr Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title_full_unstemmed Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title_short Death of new microRNA genes in Drosophila via gradual loss of fitness advantages
title_sort death of new microrna genes in drosophila via gradual loss of fitness advantages
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6120634/
https://www.ncbi.nlm.nih.gov/pubmed/30049791
http://dx.doi.org/10.1101/gr.233809.117
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