Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks

Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater eco...

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Main Authors: Jukka-Pekka Verta, Felicity C Jones
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/43785
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author Jukka-Pekka Verta
Felicity C Jones
author_facet Jukka-Pekka Verta
Felicity C Jones
author_sort Jukka-Pekka Verta
collection DOAJ
description Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that cis-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for cis-regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of cis- and trans-regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, cis-regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.
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spelling doaj.art-547b651d2de1427abc0ba15c12fadc852022-12-22T02:04:59ZengeLife Sciences Publications LtdeLife2050-084X2019-05-01810.7554/eLife.43785Predominance of cis-regulatory changes in parallel expression divergence of sticklebacksJukka-Pekka Verta0https://orcid.org/0000-0003-1701-6124Felicity C Jones1https://orcid.org/0000-0002-5027-1031Friedrich Miescher Laboratory of the Max Planck Society, Max-Planck-Ring, Tübingen, Germany; Organismal and Evolutionary Biology Research Programme, University of Helsinki, Helsinki, FinlandFriedrich Miescher Laboratory of the Max Planck Society, Max-Planck-Ring, Tübingen, GermanyRegulation of gene expression is thought to play a major role in adaptation, but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that cis-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for cis-regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of cis- and trans-regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, cis-regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.https://elifesciences.org/articles/43785gene regulationparallel evolutionselective sweepsgenetic assimilationHaldane's sievethreespine stickleback
spellingShingle Jukka-Pekka Verta
Felicity C Jones
Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
eLife
gene regulation
parallel evolution
selective sweeps
genetic assimilation
Haldane's sieve
threespine stickleback
title Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
title_full Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
title_fullStr Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
title_full_unstemmed Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
title_short Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
title_sort predominance of cis regulatory changes in parallel expression divergence of sticklebacks
topic gene regulation
parallel evolution
selective sweeps
genetic assimilation
Haldane's sieve
threespine stickleback
url https://elifesciences.org/articles/43785
work_keys_str_mv AT jukkapekkaverta predominanceofcisregulatorychangesinparallelexpressiondivergenceofsticklebacks
AT felicitycjones predominanceofcisregulatorychangesinparallelexpressiondivergenceofsticklebacks