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Neutral evolution of robustness in Drosophila microRNA precursors


Price, N; Cartwright, R A; Sabath, N; Graur, D; Azevedo, R B R (2011). Neutral evolution of robustness in Drosophila microRNA precursors. Molecular Biology and Evolution, 28(7):2115-2123.

Abstract

Mutational robustness describes the extent to which a phenotype remains unchanged in the face of mutations. Theory predicts that the strength of direct selection for mutational robustness is at most the magnitude of the rate of deleterious mutation. As far as nucleic acid sequences are concerned, only long sequences in organisms with high deleterious mutation rates and large population sizes are expected to evolve mutational robustness. Surprisingly, recent studies have concluded that molecules that meet none of these conditions--the microRNA precursors (pre-miRNAs) of multicellular eukaryotes--show signs of selection for mutational and/or environmental robustness. To resolve the apparent disagreement between theory and these studies, we have reconstructed the evolutionary history of Drosophila pre-miRNAs and compared the robustness of each sequence to that of its reconstructed ancestor. In addition, we "replayed the tape" of pre-miRNA evolution via simulation under different evolutionary assumptions and compared these alternative histories with the actual one. We found that Drosophila pre-miRNAs have evolved under strong purifying selection against changes in secondary structure. Contrary to earlier claims, there is no evidence that these RNAs have been shaped by either direct or congruent selection for any kind of robustness. Instead, the high robustness of Drosophila pre-miRNAs appears to be mostly intrinsic and likely a consequence of selection for functional structures.

Abstract

Mutational robustness describes the extent to which a phenotype remains unchanged in the face of mutations. Theory predicts that the strength of direct selection for mutational robustness is at most the magnitude of the rate of deleterious mutation. As far as nucleic acid sequences are concerned, only long sequences in organisms with high deleterious mutation rates and large population sizes are expected to evolve mutational robustness. Surprisingly, recent studies have concluded that molecules that meet none of these conditions--the microRNA precursors (pre-miRNAs) of multicellular eukaryotes--show signs of selection for mutational and/or environmental robustness. To resolve the apparent disagreement between theory and these studies, we have reconstructed the evolutionary history of Drosophila pre-miRNAs and compared the robustness of each sequence to that of its reconstructed ancestor. In addition, we "replayed the tape" of pre-miRNA evolution via simulation under different evolutionary assumptions and compared these alternative histories with the actual one. We found that Drosophila pre-miRNAs have evolved under strong purifying selection against changes in secondary structure. Contrary to earlier claims, there is no evidence that these RNAs have been shaped by either direct or congruent selection for any kind of robustness. Instead, the high robustness of Drosophila pre-miRNAs appears to be mostly intrinsic and likely a consequence of selection for functional structures.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Date:31 January 2011
Deposited On:12 Mar 2012 12:23
Last Modified:07 Aug 2017 01:51
Publisher:Oxford University Press
ISSN:0737-4038
Additional Information:This is a pre-copy-editing, author-produced PDF of an article accepted for publication in [insert journal title] following peer review. The definitive publisher-authenticated version Price, N; Cartwright, R A; Sabath, N; Graur, D; Azevedo, R B R (2011). Neutral evolution of robustness in Drosophila microRNA precursors. Molecular Biology and Evolution, 28(7):2115-2123 is available online at: http://dx.doi.org/10.1093/molbev/msr029
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1093/molbev/msr029
PubMed ID:21285032

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