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

Jukka-Pekka Verta, Felicity Jones

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Regulation of gene expression is thought to play a major role in adaptation but there are conflicting predictions for the relative importance of cis- and trans-regulatory mechanisms in the early stages adaptive divergence. Parallel evolution of marine and freshwater threespine stickleback fish provides an excellent opportunity to dissect whether the same molecular mechanisms underlie repeated adaptive divergence in gene expression. Using RNA-seq of four marine-freshwater ecotype pairs from Scotland and Canada, we first identified genes with parallel divergence in expression and show that these are found near previously reported adaptive loci and show a molecular signature of selection centered around the transcription start site. With allele-specific expression assays in F1 hybrids we next show that expression divergence is predominantly driven by cis-regulatory control in all four river systems, a pattern that is enriched in parallel divergently expressed genes. In particular, for genes whose expression is up-regulated in parallel among freshwater fish the quantitative degree of cis- and trans-regulation is also highly correlated, suggesting a shared genetic basis across populations. This stands in contrast to genes up-regulated in parallel in marine fish, whose degree of cis- and trans-regulation is less correlated and predictable. This observed asymmetry in parallelism in how genes are up-regulated in marine and freshwater fish can be explained by differences in the evolutionary contexts of the diverging ecotypes. Finally, we show that cis-regulation is predominantly additive and shows greater robustness to different in genetic backgrounds and environmental conditions. We argue that these features make cis-regulation well-poised for rapid adaptive divergence of gene expression under conditions of on-going gene flow. Combined our study highlights how natural selection on dispersed cis-regulatory elements can shape the adaptive landscape of the genome.
Original languageEnglish
Article number43785
JournaleLife
Volume8
Issue numbere43785
Number of pages30
ISSN2050-084X
DOIs
Publication statusPublished - 15 May 2019
MoE publication typeA1 Journal article-refereed

Fields of Science

  • ADAPTATION
  • ADAPTIVE EVOLUTION
  • ALLELE
  • FRESH-WATER
  • GENE-EXPRESSION
  • GENERATION
  • INSIGHTS
  • PELVIC REDUCTION
  • PLASTICITY
  • QUANTITATIVE TRAIT LOCUS
  • 1181 Ecology, evolutionary biology

Cite this

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title = "Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks",
abstract = "Regulation of gene expression is thought to play a major role in adaptation but there are conflicting predictions for the relative importance of cis- and trans-regulatory mechanisms in the early stages adaptive divergence. Parallel evolution of marine and freshwater threespine stickleback fish provides an excellent opportunity to dissect whether the same molecular mechanisms underlie repeated adaptive divergence in gene expression. Using RNA-seq of four marine-freshwater ecotype pairs from Scotland and Canada, we first identified genes with parallel divergence in expression and show that these are found near previously reported adaptive loci and show a molecular signature of selection centered around the transcription start site. With allele-specific expression assays in F1 hybrids we next show that expression divergence is predominantly driven by cis-regulatory control in all four river systems, a pattern that is enriched in parallel divergently expressed genes. In particular, for genes whose expression is up-regulated in parallel among freshwater fish the quantitative degree of cis- and trans-regulation is also highly correlated, suggesting a shared genetic basis across populations. This stands in contrast to genes up-regulated in parallel in marine fish, whose degree of cis- and trans-regulation is less correlated and predictable. This observed asymmetry in parallelism in how genes are up-regulated in marine and freshwater fish can be explained by differences in the evolutionary contexts of the diverging ecotypes. Finally, we show that cis-regulation is predominantly additive and shows greater robustness to different in genetic backgrounds and environmental conditions. We argue that these features make cis-regulation well-poised for rapid adaptive divergence of gene expression under conditions of on-going gene flow. Combined our study highlights how natural selection on dispersed cis-regulatory elements can shape the adaptive landscape of the genome.",
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author = "Jukka-Pekka Verta and Felicity Jones",
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Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. / Verta, Jukka-Pekka; Jones, Felicity.

In: eLife, Vol. 8, No. e43785, 43785, 15.05.2019.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks

AU - Verta, Jukka-Pekka

AU - Jones, Felicity

PY - 2019/5/15

Y1 - 2019/5/15

N2 - Regulation of gene expression is thought to play a major role in adaptation but there are conflicting predictions for the relative importance of cis- and trans-regulatory mechanisms in the early stages adaptive divergence. Parallel evolution of marine and freshwater threespine stickleback fish provides an excellent opportunity to dissect whether the same molecular mechanisms underlie repeated adaptive divergence in gene expression. Using RNA-seq of four marine-freshwater ecotype pairs from Scotland and Canada, we first identified genes with parallel divergence in expression and show that these are found near previously reported adaptive loci and show a molecular signature of selection centered around the transcription start site. With allele-specific expression assays in F1 hybrids we next show that expression divergence is predominantly driven by cis-regulatory control in all four river systems, a pattern that is enriched in parallel divergently expressed genes. In particular, for genes whose expression is up-regulated in parallel among freshwater fish the quantitative degree of cis- and trans-regulation is also highly correlated, suggesting a shared genetic basis across populations. This stands in contrast to genes up-regulated in parallel in marine fish, whose degree of cis- and trans-regulation is less correlated and predictable. This observed asymmetry in parallelism in how genes are up-regulated in marine and freshwater fish can be explained by differences in the evolutionary contexts of the diverging ecotypes. Finally, we show that cis-regulation is predominantly additive and shows greater robustness to different in genetic backgrounds and environmental conditions. We argue that these features make cis-regulation well-poised for rapid adaptive divergence of gene expression under conditions of on-going gene flow. Combined our study highlights how natural selection on dispersed cis-regulatory elements can shape the adaptive landscape of the genome.

AB - Regulation of gene expression is thought to play a major role in adaptation but there are conflicting predictions for the relative importance of cis- and trans-regulatory mechanisms in the early stages adaptive divergence. Parallel evolution of marine and freshwater threespine stickleback fish provides an excellent opportunity to dissect whether the same molecular mechanisms underlie repeated adaptive divergence in gene expression. Using RNA-seq of four marine-freshwater ecotype pairs from Scotland and Canada, we first identified genes with parallel divergence in expression and show that these are found near previously reported adaptive loci and show a molecular signature of selection centered around the transcription start site. With allele-specific expression assays in F1 hybrids we next show that expression divergence is predominantly driven by cis-regulatory control in all four river systems, a pattern that is enriched in parallel divergently expressed genes. In particular, for genes whose expression is up-regulated in parallel among freshwater fish the quantitative degree of cis- and trans-regulation is also highly correlated, suggesting a shared genetic basis across populations. This stands in contrast to genes up-regulated in parallel in marine fish, whose degree of cis- and trans-regulation is less correlated and predictable. This observed asymmetry in parallelism in how genes are up-regulated in marine and freshwater fish can be explained by differences in the evolutionary contexts of the diverging ecotypes. Finally, we show that cis-regulation is predominantly additive and shows greater robustness to different in genetic backgrounds and environmental conditions. We argue that these features make cis-regulation well-poised for rapid adaptive divergence of gene expression under conditions of on-going gene flow. Combined our study highlights how natural selection on dispersed cis-regulatory elements can shape the adaptive landscape of the genome.

KW - ADAPTATION

KW - ADAPTIVE EVOLUTION

KW - ALLELE

KW - FRESH-WATER

KW - GENE-EXPRESSION

KW - GENERATION

KW - INSIGHTS

KW - PELVIC REDUCTION

KW - PLASTICITY

KW - QUANTITATIVE TRAIT LOCUS

KW - 1181 Ecology, evolutionary biology

U2 - 10.7554/eLife.43785

DO - 10.7554/eLife.43785

M3 - Article

VL - 8

JO - eLife

JF - eLife

SN - 2050-084X

IS - e43785

M1 - 43785

ER -