Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)
Gene expression levels are key molecular phenotypes at the interplay between genotype and environment. Mounting evidence suggests that short‐term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of...
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Veröffentlicht in: | Molecular ecology 2022-10, Vol.31 (19), p.4949-4961 |
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description | Gene expression levels are key molecular phenotypes at the interplay between genotype and environment. Mounting evidence suggests that short‐term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of this effect, how general it is, and whether it results in parallel changes across populations are not well understood. Here, we take advantage of the well‐studied cane toad, Rhinella marina, to examine the effect of short‐term captivity on brain gene expression levels, and determine whether effects of captivity differ between long‐colonized and vanguard populations of the cane toad's Australian invasion range. We compared the transcriptomes of wild‐caught toads immediately assayed with those from toads captured from the same populations but maintained in captivity for seven months. We found large differences in gene expression levels between captive and wild‐caught toads from the same population, with an over‐representation of processes related to behaviour and the response to stress. Captivity had a much larger effect on both gene expression levels and gene expression variability in toads from vanguard populations compared to toads from long‐colonized areas, potentially indicating an increased plasticity in toads at the leading edge of the invasion. Overall, our findings indicate that short‐term captivity can induce large and population‐specific transcriptomic changes, which has significant implications for studies comparing phenotypic traits of wild‐caught organisms from different populations that have been held in captivity. |
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Mounting evidence suggests that short‐term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of this effect, how general it is, and whether it results in parallel changes across populations are not well understood. Here, we take advantage of the well‐studied cane toad, Rhinella marina, to examine the effect of short‐term captivity on brain gene expression levels, and determine whether effects of captivity differ between long‐colonized and vanguard populations of the cane toad's Australian invasion range. We compared the transcriptomes of wild‐caught toads immediately assayed with those from toads captured from the same populations but maintained in captivity for seven months. We found large differences in gene expression levels between captive and wild‐caught toads from the same population, with an over‐representation of processes related to behaviour and the response to stress. Captivity had a much larger effect on both gene expression levels and gene expression variability in toads from vanguard populations compared to toads from long‐colonized areas, potentially indicating an increased plasticity in toads at the leading edge of the invasion. Overall, our findings indicate that short‐term captivity can induce large and population‐specific transcriptomic changes, which has significant implications for studies comparing phenotypic traits of wild‐caught organisms from different populations that have been held in captivity.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.16633</identifier><identifier>PMID: 35894800</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Australia ; Brain ; Bufo marinus ; Bufo marinus - genetics ; cane toad ; Captivity ; Environmental changes ; Environmental conditions ; Gene expression ; Genotypes ; Introduced Species ; invasive species ; Original ; ORIGINAL ARTICLES ; Phenotypes ; Poaceae ; population ; Populations ; Rhinella marina ; Toads ; Transcriptome - genetics ; Transcriptomes ; Transcriptomics</subject><ispartof>Molecular ecology, 2022-10, Vol.31 (19), p.4949-4961</ispartof><rights>2022 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4433-32744bc778beb359ba3d6452095ab0bc2ebd03818ffefc5ed4448e762a147c233</citedby><cites>FETCH-LOGICAL-c4433-32744bc778beb359ba3d6452095ab0bc2ebd03818ffefc5ed4448e762a147c233</cites><orcidid>0000-0003-0466-8326 ; 0000-0002-3279-7005 ; 0000-0002-1650-0064</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.16633$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.16633$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35894800$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yagound, Boris</creatorcontrib><creatorcontrib>West, Andrea J.</creatorcontrib><creatorcontrib>Richardson, Mark F.</creatorcontrib><creatorcontrib>Gruber, Jodie</creatorcontrib><creatorcontrib>Reid, Jack G.</creatorcontrib><creatorcontrib>Whiting, Martin J.</creatorcontrib><creatorcontrib>Rollins, Lee A.</creatorcontrib><title>Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Gene expression levels are key molecular phenotypes at the interplay between genotype and environment. Mounting evidence suggests that short‐term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of this effect, how general it is, and whether it results in parallel changes across populations are not well understood. Here, we take advantage of the well‐studied cane toad, Rhinella marina, to examine the effect of short‐term captivity on brain gene expression levels, and determine whether effects of captivity differ between long‐colonized and vanguard populations of the cane toad's Australian invasion range. We compared the transcriptomes of wild‐caught toads immediately assayed with those from toads captured from the same populations but maintained in captivity for seven months. We found large differences in gene expression levels between captive and wild‐caught toads from the same population, with an over‐representation of processes related to behaviour and the response to stress. Captivity had a much larger effect on both gene expression levels and gene expression variability in toads from vanguard populations compared to toads from long‐colonized areas, potentially indicating an increased plasticity in toads at the leading edge of the invasion. Overall, our findings indicate that short‐term captivity can induce large and population‐specific transcriptomic changes, which has significant implications for studies comparing phenotypic traits of wild‐caught organisms from different populations that have been held in captivity.</description><subject>Animals</subject><subject>Australia</subject><subject>Brain</subject><subject>Bufo marinus</subject><subject>Bufo marinus - genetics</subject><subject>cane toad</subject><subject>Captivity</subject><subject>Environmental changes</subject><subject>Environmental conditions</subject><subject>Gene expression</subject><subject>Genotypes</subject><subject>Introduced Species</subject><subject>invasive species</subject><subject>Original</subject><subject>ORIGINAL ARTICLES</subject><subject>Phenotypes</subject><subject>Poaceae</subject><subject>population</subject><subject>Populations</subject><subject>Rhinella marina</subject><subject>Toads</subject><subject>Transcriptome - genetics</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc9qFTEYxYMo9lpd-AIScNMups3_yWyEcmlVqAii4C5kksy9KTPJmGQqdyH0EXxGn8TUW4sKZpPF9_tOzskB4DlGJ7ie08mZEywEpQ_AClPBG9Kxzw_BCnWCNBhJegCe5HyFEKaE88fggHLZMYnQCnxb67n4a1920Ae7GJfhqNPGQR0snOO8jLr4GH7cfLdudsG6UGCftA-wJB2ySX4ucfIGmq0Om7pdJ1_9aOuC0ctmW6DRwcEStc3w6MPWBzeOGk46-aCPn4JHgx6ze3Z3H4JPF-cf12-ay_ev367PLhvDGKUNJS1jvWlb2bue8q7X1ArGCeq47lFviOstohLLYXCD4c4yxqRrBdGYtYZQeghe7XXnpZ-cNTVF0qOak69Gdipqr_6eBL9Vm3itOolYfbYKHN0JpPhlcbmoyWdzGyW4uGRFRMeJ5LwTFX35D3oVlxRqPEVa3IpWyI5X6nhPmRRzTm64N4ORui1V1VLVr1Ir--JP9_fk7xYrcLoH6s-73f-V1Lvz9V7yJ6HPsFU</recordid><startdate>202210</startdate><enddate>202210</enddate><creator>Yagound, Boris</creator><creator>West, Andrea J.</creator><creator>Richardson, Mark F.</creator><creator>Gruber, Jodie</creator><creator>Reid, Jack G.</creator><creator>Whiting, Martin J.</creator><creator>Rollins, Lee A.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><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><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0466-8326</orcidid><orcidid>https://orcid.org/0000-0002-3279-7005</orcidid><orcidid>https://orcid.org/0000-0002-1650-0064</orcidid></search><sort><creationdate>202210</creationdate><title>Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)</title><author>Yagound, Boris ; West, Andrea J. ; Richardson, Mark F. ; Gruber, Jodie ; Reid, Jack G. ; Whiting, Martin J. ; Rollins, Lee A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4433-32744bc778beb359ba3d6452095ab0bc2ebd03818ffefc5ed4448e762a147c233</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Australia</topic><topic>Brain</topic><topic>Bufo marinus</topic><topic>Bufo marinus - genetics</topic><topic>cane toad</topic><topic>Captivity</topic><topic>Environmental changes</topic><topic>Environmental conditions</topic><topic>Gene expression</topic><topic>Genotypes</topic><topic>Introduced Species</topic><topic>invasive species</topic><topic>Original</topic><topic>ORIGINAL ARTICLES</topic><topic>Phenotypes</topic><topic>Poaceae</topic><topic>population</topic><topic>Populations</topic><topic>Rhinella marina</topic><topic>Toads</topic><topic>Transcriptome - genetics</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yagound, Boris</creatorcontrib><creatorcontrib>West, Andrea J.</creatorcontrib><creatorcontrib>Richardson, Mark F.</creatorcontrib><creatorcontrib>Gruber, Jodie</creatorcontrib><creatorcontrib>Reid, Jack G.</creatorcontrib><creatorcontrib>Whiting, Martin J.</creatorcontrib><creatorcontrib>Rollins, Lee A.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yagound, Boris</au><au>West, Andrea J.</au><au>Richardson, Mark F.</au><au>Gruber, Jodie</au><au>Reid, Jack G.</au><au>Whiting, Martin J.</au><au>Rollins, Lee A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina)</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2022-10</date><risdate>2022</risdate><volume>31</volume><issue>19</issue><spage>4949</spage><epage>4961</epage><pages>4949-4961</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Gene expression levels are key molecular phenotypes at the interplay between genotype and environment. Mounting evidence suggests that short‐term changes in environmental conditions, such as those encountered in captivity, can substantially affect gene expression levels. Yet, the exact magnitude of this effect, how general it is, and whether it results in parallel changes across populations are not well understood. Here, we take advantage of the well‐studied cane toad, Rhinella marina, to examine the effect of short‐term captivity on brain gene expression levels, and determine whether effects of captivity differ between long‐colonized and vanguard populations of the cane toad's Australian invasion range. We compared the transcriptomes of wild‐caught toads immediately assayed with those from toads captured from the same populations but maintained in captivity for seven months. We found large differences in gene expression levels between captive and wild‐caught toads from the same population, with an over‐representation of processes related to behaviour and the response to stress. Captivity had a much larger effect on both gene expression levels and gene expression variability in toads from vanguard populations compared to toads from long‐colonized areas, potentially indicating an increased plasticity in toads at the leading edge of the invasion. Overall, our findings indicate that short‐term captivity can induce large and population‐specific transcriptomic changes, which has significant implications for studies comparing phenotypic traits of wild‐caught organisms from different populations that have been held in captivity.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35894800</pmid><doi>10.1111/mec.16633</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-0466-8326</orcidid><orcidid>https://orcid.org/0000-0002-3279-7005</orcidid><orcidid>https://orcid.org/0000-0002-1650-0064</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Australia Brain Bufo marinus Bufo marinus - genetics cane toad Captivity Environmental changes Environmental conditions Gene expression Genotypes Introduced Species invasive species Original ORIGINAL ARTICLES Phenotypes Poaceae population Populations Rhinella marina Toads Transcriptome - genetics Transcriptomes Transcriptomics |
title | Captivity induces large and population‐dependent brain transcriptomic changes in wild‐caught cane toads (Rhinella marina) |
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