Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression

Abstract Novel forms of phenotypic plasticity may evolve by lineage‐specific changes or by co‐opting mechanisms from more general forms of plasticity. Here, we evaluated whether a novel resource polyphenism in New World spadefoot toads (genus Spea) evolved by co‐opting mechanisms from an ancestral f...

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Main Authors: Andrew J. Isdaner, Nicholas A. Levis, David W. Pfennig
Format: Article
Language:English
Published: Wiley 2023-10-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.10646
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author Andrew J. Isdaner
Nicholas A. Levis
David W. Pfennig
author_facet Andrew J. Isdaner
Nicholas A. Levis
David W. Pfennig
author_sort Andrew J. Isdaner
collection DOAJ
description Abstract Novel forms of phenotypic plasticity may evolve by lineage‐specific changes or by co‐opting mechanisms from more general forms of plasticity. Here, we evaluated whether a novel resource polyphenism in New World spadefoot toads (genus Spea) evolved by co‐opting mechanisms from an ancestral form of plasticity common in anurans—accelerating larval development rate in response to pond drying. We compared overlap in differentially expressed genes between alternative trophic morphs constituting the polyphenism in Spea versus those found between tadpoles of Old World spadefoot toads (genus Pelobates) when experiencing different pond‐drying regimes. Specifically, we (1) generated a de novo transcriptome and conducted differential gene expression analysis in Spea multiplicata, (2) utilized existing gene expression data and a recently published transcriptome for Pelobates cultripes when exposed to different drying regimes, and (3) identified unique and overlapping differentially expressed transcripts. We found thousands of differentially expressed genes between S. multiplicata morphs that were involved in major developmental reorganization, but the vast majority of these were not differentially expressed in P. cultripes. Thus, S. multiplicata's novel polyphenism appears to have arisen primarily through lineage‐specific changes in gene expression and not by co‐opting existing patterns of gene expression involved in pond‐drying plasticity. Therefore, although ancestral stress responses might jump‐start evolutionary innovation, substantial lineage‐specific modification might be needed to refine these responses into more complex forms of plasticity.
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spelling doaj.art-dc4c78a9518947668a606ae9b03981b82023-10-27T04:40:51ZengWileyEcology and Evolution2045-77582023-10-011310n/an/a10.1002/ece3.10646Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expressionAndrew J. Isdaner0Nicholas A. Levis1David W. Pfennig2Department of Biology University of North Carolina Chapel Hill North Carolina USADepartment of Biology University of North Carolina Chapel Hill North Carolina USADepartment of Biology University of North Carolina Chapel Hill North Carolina USAAbstract Novel forms of phenotypic plasticity may evolve by lineage‐specific changes or by co‐opting mechanisms from more general forms of plasticity. Here, we evaluated whether a novel resource polyphenism in New World spadefoot toads (genus Spea) evolved by co‐opting mechanisms from an ancestral form of plasticity common in anurans—accelerating larval development rate in response to pond drying. We compared overlap in differentially expressed genes between alternative trophic morphs constituting the polyphenism in Spea versus those found between tadpoles of Old World spadefoot toads (genus Pelobates) when experiencing different pond‐drying regimes. Specifically, we (1) generated a de novo transcriptome and conducted differential gene expression analysis in Spea multiplicata, (2) utilized existing gene expression data and a recently published transcriptome for Pelobates cultripes when exposed to different drying regimes, and (3) identified unique and overlapping differentially expressed transcripts. We found thousands of differentially expressed genes between S. multiplicata morphs that were involved in major developmental reorganization, but the vast majority of these were not differentially expressed in P. cultripes. Thus, S. multiplicata's novel polyphenism appears to have arisen primarily through lineage‐specific changes in gene expression and not by co‐opting existing patterns of gene expression involved in pond‐drying plasticity. Therefore, although ancestral stress responses might jump‐start evolutionary innovation, substantial lineage‐specific modification might be needed to refine these responses into more complex forms of plasticity.https://doi.org/10.1002/ece3.10646developmental plasticitygene expressionnoveltyphenotypic plasticityspadefoottranscriptomics
spellingShingle Andrew J. Isdaner
Nicholas A. Levis
David W. Pfennig
Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
Ecology and Evolution
developmental plasticity
gene expression
novelty
phenotypic plasticity
spadefoot
transcriptomics
title Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
title_full Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
title_fullStr Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
title_full_unstemmed Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
title_short Comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage‐specific changes in gene expression
title_sort comparative transcriptomics reveals that a novel form of phenotypic plasticity evolved via lineage specific changes in gene expression
topic developmental plasticity
gene expression
novelty
phenotypic plasticity
spadefoot
transcriptomics
url https://doi.org/10.1002/ece3.10646
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AT davidwpfennig comparativetranscriptomicsrevealsthatanovelformofphenotypicplasticityevolvedvialineagespecificchangesingeneexpression