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Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia
Research has shown that a change in environmental conditions can alter the expression of traits during development (i.e., “within‐generation phenotypic plasticity”) as well as induce heritable phenotypic responses that persist for multiple generations (i.e., “transgenerational plasticity”, TGP). It...
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Published in: | Molecular ecology 2017-10, Vol.26 (19), p.5003-5015 |
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description | Research has shown that a change in environmental conditions can alter the expression of traits during development (i.e., “within‐generation phenotypic plasticity”) as well as induce heritable phenotypic responses that persist for multiple generations (i.e., “transgenerational plasticity”, TGP). It has long been assumed that shifts in gene expression are tightly linked to observed trait responses at the phenotypic level. Yet, the manner in which organisms couple within‐ and TGP at the molecular level is unclear. Here we tested the influence of fish predator chemical cues on patterns of gene expression within‐ and across generations using a clone of Daphnia ambigua that is known to exhibit strong TGP but weak within‐generation plasticity. Daphnia were reared in the presence of predator cues in generation 1, and shifts in gene expression were tracked across two additional asexual experimental generations that lacked exposure to predator cues. Initial exposure to predator cues in generation 1 was linked to ~50 responsive genes, but such shifts were 3–4× larger in later generations. Differentially expressed genes included those involved in reproduction, exoskeleton structure and digestion; major shifts in expression of genes encoding ribosomal proteins were also identified. Furthermore, shifts within the first‐generation and transgenerational shifts in gene expression were largely distinct in terms of the genes that were differentially expressed. Such results argue that the gene expression programmes involved in within‐ vs. transgeneration plasticity are fundamentally different. Our study provides new key insights into the plasticity of gene expression and how it relates to phenotypic plasticity in nature.
see also the Perspective by Bell and Stein |
doi_str_mv | 10.1111/mec.14213 |
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see also the Perspective by Bell and Stein</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.14213</identifier><identifier>PMID: 28628257</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Chemical stimuli ; Cues ; Daphnia ; Daphnia - genetics ; ecoresponsive ; Environment ; Environmental changes ; Environmental conditions ; epigenetics ; Exoskeleton ; Exposure ; Fishes ; Food Chain ; Gene Expression ; Genes ; Inheritance Patterns ; Phenotype ; Phenotypic plasticity ; Plastic properties ; Plasticity ; Predatory Behavior ; Proteins ; Ribosomal proteins ; transcriptomics ; transgenerational plasticity ; water fleas</subject><ispartof>Molecular ecology, 2017-10, Vol.26 (19), p.5003-5015</ispartof><rights>2017 John Wiley & Sons Ltd</rights><rights>2017 John Wiley & Sons Ltd.</rights><rights>Copyright © 2017 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3533-251287ea8a3a340113c6eb35579ea7a0e5f46976f82b0ef12183a79684ea21c53</citedby><cites>FETCH-LOGICAL-c3533-251287ea8a3a340113c6eb35579ea7a0e5f46976f82b0ef12183a79684ea21c53</cites><orcidid>0000-0002-5912-1574</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28628257$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hales, Nicole R.</creatorcontrib><creatorcontrib>Schield, Drew R.</creatorcontrib><creatorcontrib>Andrew, Audra L.</creatorcontrib><creatorcontrib>Card, Daren C.</creatorcontrib><creatorcontrib>Walsh, Matthew R.</creatorcontrib><creatorcontrib>Castoe, Todd A.</creatorcontrib><title>Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Research has shown that a change in environmental conditions can alter the expression of traits during development (i.e., “within‐generation phenotypic plasticity”) as well as induce heritable phenotypic responses that persist for multiple generations (i.e., “transgenerational plasticity”, TGP). It has long been assumed that shifts in gene expression are tightly linked to observed trait responses at the phenotypic level. Yet, the manner in which organisms couple within‐ and TGP at the molecular level is unclear. Here we tested the influence of fish predator chemical cues on patterns of gene expression within‐ and across generations using a clone of Daphnia ambigua that is known to exhibit strong TGP but weak within‐generation plasticity. Daphnia were reared in the presence of predator cues in generation 1, and shifts in gene expression were tracked across two additional asexual experimental generations that lacked exposure to predator cues. Initial exposure to predator cues in generation 1 was linked to ~50 responsive genes, but such shifts were 3–4× larger in later generations. Differentially expressed genes included those involved in reproduction, exoskeleton structure and digestion; major shifts in expression of genes encoding ribosomal proteins were also identified. Furthermore, shifts within the first‐generation and transgenerational shifts in gene expression were largely distinct in terms of the genes that were differentially expressed. Such results argue that the gene expression programmes involved in within‐ vs. transgeneration plasticity are fundamentally different. Our study provides new key insights into the plasticity of gene expression and how it relates to phenotypic plasticity in nature.
see also the Perspective by Bell and Stein</description><subject>Animals</subject><subject>Chemical stimuli</subject><subject>Cues</subject><subject>Daphnia</subject><subject>Daphnia - genetics</subject><subject>ecoresponsive</subject><subject>Environment</subject><subject>Environmental changes</subject><subject>Environmental conditions</subject><subject>epigenetics</subject><subject>Exoskeleton</subject><subject>Exposure</subject><subject>Fishes</subject><subject>Food Chain</subject><subject>Gene Expression</subject><subject>Genes</subject><subject>Inheritance Patterns</subject><subject>Phenotype</subject><subject>Phenotypic plasticity</subject><subject>Plastic properties</subject><subject>Plasticity</subject><subject>Predatory Behavior</subject><subject>Proteins</subject><subject>Ribosomal proteins</subject><subject>transcriptomics</subject><subject>transgenerational plasticity</subject><subject>water fleas</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNp1kcFu1DAQhi0EokvhwAsgS1zgkNZjx4lzREsLSEVcQOIWzTqTXVeJHexEZW-ceuYZeRLc3cIBCV8seT5_M6OfsecgziCf85HsGZQS1AO2AlXpQjbl14dsJZpKFiCMOmFPUroWApTU-jE7kaaSRup6xW7Xwc8R0-z8lm_JE6fvU6SUXPB8imEbcUzchpjfpuA7fuPmXS5Qh3OIv378dL5bLHV82pEP835ylk_Dnc-6eX-gneeYP6KNIaVDj4hz1ieeK29x2nmHT9mjHodEz-7vU_bl8uLz-n1x9endh_Wbq8IqrVQhNUhTExpUqEoBoGxFG6V13RDWKEj3ZdXUVW_kRlAPEozCuqlMSSjBanXKXh29ebVvC6W5HV2yNAzoKSyphQZAClGJOqMv_0GvwxJ9ni5TWoksNSJTr4_UYbtIfTtFN2LctyDau3DaHE57CCezL-6Ny2ak7i_5J40MnB-BGzfQ_v-m9uPF-qj8DQpUm7Q</recordid><startdate>201710</startdate><enddate>201710</enddate><creator>Hales, Nicole R.</creator><creator>Schield, Drew R.</creator><creator>Andrew, Audra L.</creator><creator>Card, Daren C.</creator><creator>Walsh, Matthew R.</creator><creator>Castoe, Todd A.</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5912-1574</orcidid></search><sort><creationdate>201710</creationdate><title>Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia</title><author>Hales, Nicole R. ; Schield, Drew R. ; Andrew, Audra L. ; Card, Daren C. ; Walsh, Matthew R. ; Castoe, Todd A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3533-251287ea8a3a340113c6eb35579ea7a0e5f46976f82b0ef12183a79684ea21c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Chemical stimuli</topic><topic>Cues</topic><topic>Daphnia</topic><topic>Daphnia - genetics</topic><topic>ecoresponsive</topic><topic>Environment</topic><topic>Environmental changes</topic><topic>Environmental conditions</topic><topic>epigenetics</topic><topic>Exoskeleton</topic><topic>Exposure</topic><topic>Fishes</topic><topic>Food Chain</topic><topic>Gene Expression</topic><topic>Genes</topic><topic>Inheritance Patterns</topic><topic>Phenotype</topic><topic>Phenotypic plasticity</topic><topic>Plastic properties</topic><topic>Plasticity</topic><topic>Predatory Behavior</topic><topic>Proteins</topic><topic>Ribosomal proteins</topic><topic>transcriptomics</topic><topic>transgenerational plasticity</topic><topic>water fleas</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hales, Nicole R.</creatorcontrib><creatorcontrib>Schield, Drew R.</creatorcontrib><creatorcontrib>Andrew, Audra L.</creatorcontrib><creatorcontrib>Card, Daren C.</creatorcontrib><creatorcontrib>Walsh, Matthew R.</creatorcontrib><creatorcontrib>Castoe, Todd A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hales, Nicole R.</au><au>Schield, Drew R.</au><au>Andrew, Audra L.</au><au>Card, Daren C.</au><au>Walsh, Matthew R.</au><au>Castoe, Todd A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2017-10</date><risdate>2017</risdate><volume>26</volume><issue>19</issue><spage>5003</spage><epage>5015</epage><pages>5003-5015</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Research has shown that a change in environmental conditions can alter the expression of traits during development (i.e., “within‐generation phenotypic plasticity”) as well as induce heritable phenotypic responses that persist for multiple generations (i.e., “transgenerational plasticity”, TGP). It has long been assumed that shifts in gene expression are tightly linked to observed trait responses at the phenotypic level. Yet, the manner in which organisms couple within‐ and TGP at the molecular level is unclear. Here we tested the influence of fish predator chemical cues on patterns of gene expression within‐ and across generations using a clone of Daphnia ambigua that is known to exhibit strong TGP but weak within‐generation plasticity. Daphnia were reared in the presence of predator cues in generation 1, and shifts in gene expression were tracked across two additional asexual experimental generations that lacked exposure to predator cues. Initial exposure to predator cues in generation 1 was linked to ~50 responsive genes, but such shifts were 3–4× larger in later generations. Differentially expressed genes included those involved in reproduction, exoskeleton structure and digestion; major shifts in expression of genes encoding ribosomal proteins were also identified. Furthermore, shifts within the first‐generation and transgenerational shifts in gene expression were largely distinct in terms of the genes that were differentially expressed. Such results argue that the gene expression programmes involved in within‐ vs. transgeneration plasticity are fundamentally different. Our study provides new key insights into the plasticity of gene expression and how it relates to phenotypic plasticity in nature.
see also the Perspective by Bell and Stein</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28628257</pmid><doi>10.1111/mec.14213</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-5912-1574</orcidid></addata></record> |
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subjects | Animals Chemical stimuli Cues Daphnia Daphnia - genetics ecoresponsive Environment Environmental changes Environmental conditions epigenetics Exoskeleton Exposure Fishes Food Chain Gene Expression Genes Inheritance Patterns Phenotype Phenotypic plasticity Plastic properties Plasticity Predatory Behavior Proteins Ribosomal proteins transcriptomics transgenerational plasticity water fleas |
title | Contrasting gene expression programs correspond with predator‐induced phenotypic plasticity within and across generations in Daphnia |
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