Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.

The widespread occurrence of phenotypic plasticity across all domains of life demonstrates its evolutionary significance. However, how plasticity itself evolves and how it contributes to evolution is poorly understood. Here, we investigate the predatory nematode Pristionchus pacificus with its feedi...

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Main Authors: Mohannad Dardiry, Gabi Eberhard, Hanh Witte, Christian Rödelsperger, James W Lightfoot, Ralf J Sommer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-08-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002270
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author Mohannad Dardiry
Gabi Eberhard
Hanh Witte
Christian Rödelsperger
James W Lightfoot
Ralf J Sommer
author_facet Mohannad Dardiry
Gabi Eberhard
Hanh Witte
Christian Rödelsperger
James W Lightfoot
Ralf J Sommer
author_sort Mohannad Dardiry
collection DOAJ
description The widespread occurrence of phenotypic plasticity across all domains of life demonstrates its evolutionary significance. However, how plasticity itself evolves and how it contributes to evolution is poorly understood. Here, we investigate the predatory nematode Pristionchus pacificus with its feeding structure plasticity using recombinant-inbred-line and quantitative-trait-locus (QTL) analyses between natural isolates. We show that a single QTL at a core developmental gene controls the expression of the cannibalistic morph. This QTL is composed of several cis-regulatory elements. Through CRISPR/Cas-9 engineering, we identify copy number variation of potential transcription factor binding sites that interacts with a single intronic nucleotide polymorphism. Another intronic element eliminates gene expression altogether, mimicking knockouts of the locus. Comparisons of additional isolates further support the rapid evolution of these cis-regulatory elements. Finally, an independent QTL study reveals evidence for parallel evolution at the same locus. Thus, combinations of cis-regulatory elements shape plastic trait expression and control nematode cannibalism.
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spelling doaj.art-ef410d0c46e8499483a90a63527994b42023-10-02T12:17:29ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-08-01218e300227010.1371/journal.pbio.3002270Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.Mohannad DardiryGabi EberhardHanh WitteChristian RödelspergerJames W LightfootRalf J SommerThe widespread occurrence of phenotypic plasticity across all domains of life demonstrates its evolutionary significance. However, how plasticity itself evolves and how it contributes to evolution is poorly understood. Here, we investigate the predatory nematode Pristionchus pacificus with its feeding structure plasticity using recombinant-inbred-line and quantitative-trait-locus (QTL) analyses between natural isolates. We show that a single QTL at a core developmental gene controls the expression of the cannibalistic morph. This QTL is composed of several cis-regulatory elements. Through CRISPR/Cas-9 engineering, we identify copy number variation of potential transcription factor binding sites that interacts with a single intronic nucleotide polymorphism. Another intronic element eliminates gene expression altogether, mimicking knockouts of the locus. Comparisons of additional isolates further support the rapid evolution of these cis-regulatory elements. Finally, an independent QTL study reveals evidence for parallel evolution at the same locus. Thus, combinations of cis-regulatory elements shape plastic trait expression and control nematode cannibalism.https://doi.org/10.1371/journal.pbio.3002270
spellingShingle Mohannad Dardiry
Gabi Eberhard
Hanh Witte
Christian Rödelsperger
James W Lightfoot
Ralf J Sommer
Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
PLoS Biology
title Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
title_full Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
title_fullStr Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
title_full_unstemmed Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
title_short Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity.
title_sort divergent combinations of cis regulatory elements control the evolution of phenotypic plasticity
url https://doi.org/10.1371/journal.pbio.3002270
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