Comparative transcriptomics reveals domestication‐associated features of Atlantic salmon lipid metabolism
Domestication of animals imposes strong targeted selection for desired traits but can also result in unintended selection due to new domestic environments. Atlantic salmon (Salmo salmar) was domesticated in the 1970s and has subsequently been selected for faster growth in systematic breeding program...
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Veröffentlicht in: | Molecular ecology 2020-05, Vol.29 (10), p.1860-1872 |
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creator | Jin, Yang Olsen, Rolf Erik Harvey, Thomas Nelson Østensen, Mari‐Ann Li, Keshuai Santi, Nina Vadstein, Olav Bones, Atle Magnar Vik, Jon Olav Sandve, Simen Rød Olsen, Yngvar |
description | Domestication of animals imposes strong targeted selection for desired traits but can also result in unintended selection due to new domestic environments. Atlantic salmon (Salmo salmar) was domesticated in the 1970s and has subsequently been selected for faster growth in systematic breeding programmes. More recently, salmon aquaculture has replaced fish oils (FOs) with vegetable oils (VOs) in feed, radically changing the levels of essential long‐chain polyunsaturated fatty acids (LC‐PUFAs). Our aim here was to study the impact of domestication on metabolism and explore the hypothesis that the shift to VO diets has unintentionally selected for a domestication‐specific lipid metabolism. We conducted a 96‐day feeding trial of domesticated and wild salmon fed diets based on FOs, VOs or phospholipids, and compared transcriptomes and fatty acids in tissues involved in lipid absorption (pyloric caeca) and lipid turnover and synthesis (liver). Domesticated salmon had faster growth and higher gene expression in glucose and lipid metabolism compared to wild fish, possibly linked to differences in regulation of circadian rhythm pathways. Only the domesticated salmon increased expression of LC‐PUFA synthesis genes when given VOs. This transcriptome response difference was mirrored at the physiological level, with domesticated salmon having higher LC‐PUFA levels but lower 18:3n‐3 and 18:2n‐6 levels. In line with this, the VO diet decreased growth rate in wild but not domesticated salmon. Our study revealed a clear impact of domestication on transcriptomic regulation linked to metabolism and suggests that unintentional selection in the domestic environment has resulted in evolution of stronger compensatory mechanisms to a diet low in LC‐PUFAs. |
doi_str_mv | 10.1111/mec.15446 |
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Atlantic salmon (Salmo salmar) was domesticated in the 1970s and has subsequently been selected for faster growth in systematic breeding programmes. More recently, salmon aquaculture has replaced fish oils (FOs) with vegetable oils (VOs) in feed, radically changing the levels of essential long‐chain polyunsaturated fatty acids (LC‐PUFAs). Our aim here was to study the impact of domestication on metabolism and explore the hypothesis that the shift to VO diets has unintentionally selected for a domestication‐specific lipid metabolism. We conducted a 96‐day feeding trial of domesticated and wild salmon fed diets based on FOs, VOs or phospholipids, and compared transcriptomes and fatty acids in tissues involved in lipid absorption (pyloric caeca) and lipid turnover and synthesis (liver). Domesticated salmon had faster growth and higher gene expression in glucose and lipid metabolism compared to wild fish, possibly linked to differences in regulation of circadian rhythm pathways. Only the domesticated salmon increased expression of LC‐PUFA synthesis genes when given VOs. This transcriptome response difference was mirrored at the physiological level, with domesticated salmon having higher LC‐PUFA levels but lower 18:3n‐3 and 18:2n‐6 levels. In line with this, the VO diet decreased growth rate in wild but not domesticated salmon. Our study revealed a clear impact of domestication on transcriptomic regulation linked to metabolism and suggests that unintentional selection in the domestic environment has resulted in evolution of stronger compensatory mechanisms to a diet low in LC‐PUFAs.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.15446</identifier><identifier>PMID: 32293070</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Aquaculture ; Breeding ; circadian regulation ; Circadian rhythms ; Diet ; Domestication ; Fatty acids ; Fish oils ; Gene expression ; Glucose metabolism ; Growth rate ; Levels ; Lipid metabolism ; Lipid turnover ; Lipids ; long‐chain polyunsaturated fatty acids ; Metabolism ; Nutrient deficiency ; Phospholipids ; Polyunsaturated fatty acids ; Salmo salar ; Salmon ; Synthesis ; transcriptomics ; vegetable oil ; Vegetable oils ; wild salmon</subject><ispartof>Molecular ecology, 2020-05, Vol.29 (10), p.1860-1872</ispartof><rights>2020 The Authors. published by John Wiley & Sons Ltd</rights><rights>2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by/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-c3886-e1b53ce6c9907c4f663a6ec51ee420c079fb603ed492d52af8fbeaef798d6cfe3</citedby><cites>FETCH-LOGICAL-c3886-e1b53ce6c9907c4f663a6ec51ee420c079fb603ed492d52af8fbeaef798d6cfe3</cites><orcidid>0000-0003-4989-5311 ; 0000-0002-7778-4515 ; 0000-0001-5597-8397</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.15446$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.15446$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32293070$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jin, Yang</creatorcontrib><creatorcontrib>Olsen, Rolf Erik</creatorcontrib><creatorcontrib>Harvey, Thomas Nelson</creatorcontrib><creatorcontrib>Østensen, Mari‐Ann</creatorcontrib><creatorcontrib>Li, Keshuai</creatorcontrib><creatorcontrib>Santi, Nina</creatorcontrib><creatorcontrib>Vadstein, Olav</creatorcontrib><creatorcontrib>Bones, Atle Magnar</creatorcontrib><creatorcontrib>Vik, Jon Olav</creatorcontrib><creatorcontrib>Sandve, Simen Rød</creatorcontrib><creatorcontrib>Olsen, Yngvar</creatorcontrib><title>Comparative transcriptomics reveals domestication‐associated features of Atlantic salmon lipid metabolism</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Domestication of animals imposes strong targeted selection for desired traits but can also result in unintended selection due to new domestic environments. Atlantic salmon (Salmo salmar) was domesticated in the 1970s and has subsequently been selected for faster growth in systematic breeding programmes. More recently, salmon aquaculture has replaced fish oils (FOs) with vegetable oils (VOs) in feed, radically changing the levels of essential long‐chain polyunsaturated fatty acids (LC‐PUFAs). Our aim here was to study the impact of domestication on metabolism and explore the hypothesis that the shift to VO diets has unintentionally selected for a domestication‐specific lipid metabolism. We conducted a 96‐day feeding trial of domesticated and wild salmon fed diets based on FOs, VOs or phospholipids, and compared transcriptomes and fatty acids in tissues involved in lipid absorption (pyloric caeca) and lipid turnover and synthesis (liver). Domesticated salmon had faster growth and higher gene expression in glucose and lipid metabolism compared to wild fish, possibly linked to differences in regulation of circadian rhythm pathways. Only the domesticated salmon increased expression of LC‐PUFA synthesis genes when given VOs. This transcriptome response difference was mirrored at the physiological level, with domesticated salmon having higher LC‐PUFA levels but lower 18:3n‐3 and 18:2n‐6 levels. In line with this, the VO diet decreased growth rate in wild but not domesticated salmon. 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Olsen, Rolf Erik ; Harvey, Thomas Nelson ; Østensen, Mari‐Ann ; Li, Keshuai ; Santi, Nina ; Vadstein, Olav ; Bones, Atle Magnar ; Vik, Jon Olav ; Sandve, Simen Rød ; Olsen, Yngvar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3886-e1b53ce6c9907c4f663a6ec51ee420c079fb603ed492d52af8fbeaef798d6cfe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aquaculture</topic><topic>Breeding</topic><topic>circadian regulation</topic><topic>Circadian rhythms</topic><topic>Diet</topic><topic>Domestication</topic><topic>Fatty acids</topic><topic>Fish oils</topic><topic>Gene expression</topic><topic>Glucose metabolism</topic><topic>Growth rate</topic><topic>Levels</topic><topic>Lipid metabolism</topic><topic>Lipid turnover</topic><topic>Lipids</topic><topic>long‐chain polyunsaturated fatty acids</topic><topic>Metabolism</topic><topic>Nutrient deficiency</topic><topic>Phospholipids</topic><topic>Polyunsaturated fatty acids</topic><topic>Salmo salar</topic><topic>Salmon</topic><topic>Synthesis</topic><topic>transcriptomics</topic><topic>vegetable oil</topic><topic>Vegetable oils</topic><topic>wild salmon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jin, Yang</creatorcontrib><creatorcontrib>Olsen, Rolf Erik</creatorcontrib><creatorcontrib>Harvey, Thomas Nelson</creatorcontrib><creatorcontrib>Østensen, Mari‐Ann</creatorcontrib><creatorcontrib>Li, Keshuai</creatorcontrib><creatorcontrib>Santi, Nina</creatorcontrib><creatorcontrib>Vadstein, Olav</creatorcontrib><creatorcontrib>Bones, Atle Magnar</creatorcontrib><creatorcontrib>Vik, Jon Olav</creatorcontrib><creatorcontrib>Sandve, Simen Rød</creatorcontrib><creatorcontrib>Olsen, Yngvar</creatorcontrib><collection>Wiley Online Library Open Access</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>Jin, Yang</au><au>Olsen, Rolf Erik</au><au>Harvey, Thomas Nelson</au><au>Østensen, Mari‐Ann</au><au>Li, Keshuai</au><au>Santi, Nina</au><au>Vadstein, Olav</au><au>Bones, Atle Magnar</au><au>Vik, Jon Olav</au><au>Sandve, Simen Rød</au><au>Olsen, Yngvar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative transcriptomics reveals domestication‐associated features of Atlantic salmon lipid metabolism</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2020-05</date><risdate>2020</risdate><volume>29</volume><issue>10</issue><spage>1860</spage><epage>1872</epage><pages>1860-1872</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Domestication of animals imposes strong targeted selection for desired traits but can also result in unintended selection due to new domestic environments. 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Only the domesticated salmon increased expression of LC‐PUFA synthesis genes when given VOs. This transcriptome response difference was mirrored at the physiological level, with domesticated salmon having higher LC‐PUFA levels but lower 18:3n‐3 and 18:2n‐6 levels. In line with this, the VO diet decreased growth rate in wild but not domesticated salmon. Our study revealed a clear impact of domestication on transcriptomic regulation linked to metabolism and suggests that unintentional selection in the domestic environment has resulted in evolution of stronger compensatory mechanisms to a diet low in LC‐PUFAs.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32293070</pmid><doi>10.1111/mec.15446</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-4989-5311</orcidid><orcidid>https://orcid.org/0000-0002-7778-4515</orcidid><orcidid>https://orcid.org/0000-0001-5597-8397</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aquaculture Breeding circadian regulation Circadian rhythms Diet Domestication Fatty acids Fish oils Gene expression Glucose metabolism Growth rate Levels Lipid metabolism Lipid turnover Lipids long‐chain polyunsaturated fatty acids Metabolism Nutrient deficiency Phospholipids Polyunsaturated fatty acids Salmo salar Salmon Synthesis transcriptomics vegetable oil Vegetable oils wild salmon |
title | Comparative transcriptomics reveals domestication‐associated features of Atlantic salmon lipid metabolism |
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