Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements

Transposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX element dispersed 77 functional but suboptimal binding sites for the dosage compensation complex to a newly formed X chromosome in Drosophila. Here we identify two linked refining mutations wit...

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Main Authors: Christopher E Ellison, Doris Bachtrog
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/05899
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author Christopher E Ellison
Doris Bachtrog
author_facet Christopher E Ellison
Doris Bachtrog
author_sort Christopher E Ellison
collection DOAJ
description Transposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX element dispersed 77 functional but suboptimal binding sites for the dosage compensation complex to a newly formed X chromosome in Drosophila. Here we identify two linked refining mutations within ISX that interact epistatically to increase binding affinity to the dosage compensation complex. Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%. Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to ‘crowd-source’ refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection. These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.
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spelling doaj.art-77a01e211c1548ecb1a6c3daf038dd8d2022-12-22T04:32:42ZengeLife Sciences Publications LtdeLife2050-084X2015-02-01410.7554/eLife.05899Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elementsChristopher E Ellison0Doris Bachtrog1Department of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesTransposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX element dispersed 77 functional but suboptimal binding sites for the dosage compensation complex to a newly formed X chromosome in Drosophila. Here we identify two linked refining mutations within ISX that interact epistatically to increase binding affinity to the dosage compensation complex. Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%. Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to ‘crowd-source’ refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection. These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.https://elifesciences.org/articles/05899Drosophila mirandatransposable elementnon-allelic gene conversionregulatory network
spellingShingle Christopher E Ellison
Doris Bachtrog
Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
eLife
Drosophila miranda
transposable element
non-allelic gene conversion
regulatory network
title Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
title_full Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
title_fullStr Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
title_full_unstemmed Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
title_short Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
title_sort non allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
topic Drosophila miranda
transposable element
non-allelic gene conversion
regulatory network
url https://elifesciences.org/articles/05899
work_keys_str_mv AT christophereellison nonallelicgeneconversionenablesrapidevolutionarychangeatmultipleregulatorysitesencodedbytransposableelements
AT dorisbachtrog nonallelicgeneconversionenablesrapidevolutionarychangeatmultipleregulatorysitesencodedbytransposableelements