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Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets
Multigenerational exposure is needed to assess the evolutionary potential of organisms in the rapidly changing seascape. Here, we investigate if there is a transgenerational effect of ocean acidification exposure on a calyptraeid gastropod such that long‐term exposure elevates offspring resilience....
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Published in: | Global change biology 2021-07, Vol.27 (14), p.3272-3281 |
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description | Multigenerational exposure is needed to assess the evolutionary potential of organisms in the rapidly changing seascape. Here, we investigate if there is a transgenerational effect of ocean acidification exposure on a calyptraeid gastropod such that long‐term exposure elevates offspring resilience. Larvae from wild type Crepidula onyx adults were reared from hatching until sexual maturity for over 36 months under three pH conditions (pH 7.3, 7.7, and 8.0). While the survivorship, growth, and respiration rate of F1 larvae were unaffected by acute ocean acidification (OA), long‐term and whole life cycle exposure significantly compromised adult survivorship, growth, and reproductive output of the slipper limpets. When kept under low pH throughout their life cycle, only 6% of the F1 slipper limpets survived pH 7.3 conditions after ~2.5 years and the number of larvae they released was ~10% of those released by the control. However, the F2 progeny from adults kept under the long‐term low pH condition hatched at a comparable size to those in medium and control pH conditions. More importantly, these F2 progeny from low pH adults outperformed F2 slipper limpets from control conditions; they had higher larval survivorship and growth, and reduced respiration rate across pH conditions, even at the extreme low pH of 7.0. The intragenerational negative consequences of OA during long‐term acclimation highlights potential carryover effects and ontogenetic shifts in stress vulnerability, especially prior to and during reproduction. Yet, the presence of a transgenerational effect implies that this slipper limpet, which has been widely introduced along the West Pacific coasts, has the potential to adapt to rapid acidification.
Slipper limpet larvae were previously shown to be resilient to ocean acidification (OA). However, whole life cycle exposure (from larvae to adult) to OA conditions reduced survivorship, growth, and reproductive output. OA exposure had a transgenerational effect such that larvae descend from OA exposed adults performed better under low pH conditions. |
doi_str_mv | 10.1111/gcb.15647 |
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Slipper limpet larvae were previously shown to be resilient to ocean acidification (OA). However, whole life cycle exposure (from larvae to adult) to OA conditions reduced survivorship, growth, and reproductive output. OA exposure had a transgenerational effect such that larvae descend from OA exposed adults performed better under low pH conditions.</description><identifier>ISSN: 1354-1013</identifier><identifier>EISSN: 1365-2486</identifier><identifier>DOI: 10.1111/gcb.15647</identifier><identifier>PMID: 33872435</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Acclimation ; Acclimatization ; Acidification ; Adults ; anthropogenic stress ; carryover effect ; Control ; Exposure ; Growth ; Hatching ; Larvae ; Life cycle ; Life cycles ; Marine molluscs ; non‐indigenous species ; Ocean acidification ; Offspring ; Ontogeny ; pH control ; pH effects ; phenotypic plasticity ; Progeny ; Respiration ; Sexual maturity ; Survival ; Vulnerability</subject><ispartof>Global change biology, 2021-07, Vol.27 (14), p.3272-3281</ispartof><rights>2021 John Wiley & Sons Ltd</rights><rights>2021 John Wiley & Sons Ltd.</rights><rights>Copyright © 2021 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3537-c189fe393048e7a79283c5ed43804777ea5507adf808840852bc1864f7464d1b3</citedby><cites>FETCH-LOGICAL-c3537-c189fe393048e7a79283c5ed43804777ea5507adf808840852bc1864f7464d1b3</cites><orcidid>0000-0002-7775-4383</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/33872435$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Maboloc, Elizaldy A.</creatorcontrib><creatorcontrib>Chan, Kit Yu Karen</creatorcontrib><title>Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets</title><title>Global change biology</title><addtitle>Glob Chang Biol</addtitle><description>Multigenerational exposure is needed to assess the evolutionary potential of organisms in the rapidly changing seascape. Here, we investigate if there is a transgenerational effect of ocean acidification exposure on a calyptraeid gastropod such that long‐term exposure elevates offspring resilience. Larvae from wild type Crepidula onyx adults were reared from hatching until sexual maturity for over 36 months under three pH conditions (pH 7.3, 7.7, and 8.0). While the survivorship, growth, and respiration rate of F1 larvae were unaffected by acute ocean acidification (OA), long‐term and whole life cycle exposure significantly compromised adult survivorship, growth, and reproductive output of the slipper limpets. When kept under low pH throughout their life cycle, only 6% of the F1 slipper limpets survived pH 7.3 conditions after ~2.5 years and the number of larvae they released was ~10% of those released by the control. However, the F2 progeny from adults kept under the long‐term low pH condition hatched at a comparable size to those in medium and control pH conditions. More importantly, these F2 progeny from low pH adults outperformed F2 slipper limpets from control conditions; they had higher larval survivorship and growth, and reduced respiration rate across pH conditions, even at the extreme low pH of 7.0. The intragenerational negative consequences of OA during long‐term acclimation highlights potential carryover effects and ontogenetic shifts in stress vulnerability, especially prior to and during reproduction. Yet, the presence of a transgenerational effect implies that this slipper limpet, which has been widely introduced along the West Pacific coasts, has the potential to adapt to rapid acidification.
Slipper limpet larvae were previously shown to be resilient to ocean acidification (OA). However, whole life cycle exposure (from larvae to adult) to OA conditions reduced survivorship, growth, and reproductive output. OA exposure had a transgenerational effect such that larvae descend from OA exposed adults performed better under low pH conditions.</description><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Acidification</subject><subject>Adults</subject><subject>anthropogenic stress</subject><subject>carryover effect</subject><subject>Control</subject><subject>Exposure</subject><subject>Growth</subject><subject>Hatching</subject><subject>Larvae</subject><subject>Life cycle</subject><subject>Life cycles</subject><subject>Marine molluscs</subject><subject>non‐indigenous species</subject><subject>Ocean acidification</subject><subject>Offspring</subject><subject>Ontogeny</subject><subject>pH control</subject><subject>pH effects</subject><subject>phenotypic plasticity</subject><subject>Progeny</subject><subject>Respiration</subject><subject>Sexual maturity</subject><subject>Survival</subject><subject>Vulnerability</subject><issn>1354-1013</issn><issn>1365-2486</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1kE1PwyAYgInRuPlx8A8YEi966AYFCjvq4leyRA96bhh9qyy0VGgz9-9Fpx5M5MIb8vDkzYPQCSUTms70xSwnVBRc7qAxZYXIcq6K3c9Z8IwSykboIMYVIYTlpNhHI8aUzDkTY_T6qAO0vXZ4_eodYGdrwGZj0gjvnY9DANz4anC6h4i74F-g3eAAsfNtTC-9x96AbrE2trK1Nbq3vsW2xdHZroOQjE0HfTxCe7V2EY6_70P0fHP9NL_LFg-39_PLRWaYYDIzVM1qYDNGuAKp5SxXzAioOFOESylBC0GkrmpFlOJEiXyZvhS8lrzgFV2yQ3S-9aZd3waIfdnYaMA53YIfYpmLVEoVSZLQsz_oyg-hTdslihNOmSxooi62lAk-xgB12QXb6LApKSk_85cpf_mVP7Gn38Zh2UD1S_70TsB0C6ytg83_pvJ2frVVfgAPUY42</recordid><startdate>202107</startdate><enddate>202107</enddate><creator>Maboloc, Elizaldy A.</creator><creator>Chan, Kit Yu Karen</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7UA</scope><scope>C1K</scope><scope>F1W</scope><scope>H97</scope><scope>L.G</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7775-4383</orcidid></search><sort><creationdate>202107</creationdate><title>Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets</title><author>Maboloc, Elizaldy A. ; Chan, Kit Yu Karen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3537-c189fe393048e7a79283c5ed43804777ea5507adf808840852bc1864f7464d1b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Acidification</topic><topic>Adults</topic><topic>anthropogenic stress</topic><topic>carryover effect</topic><topic>Control</topic><topic>Exposure</topic><topic>Growth</topic><topic>Hatching</topic><topic>Larvae</topic><topic>Life cycle</topic><topic>Life cycles</topic><topic>Marine molluscs</topic><topic>non‐indigenous species</topic><topic>Ocean acidification</topic><topic>Offspring</topic><topic>Ontogeny</topic><topic>pH control</topic><topic>pH effects</topic><topic>phenotypic plasticity</topic><topic>Progeny</topic><topic>Respiration</topic><topic>Sexual maturity</topic><topic>Survival</topic><topic>Vulnerability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Maboloc, Elizaldy A.</creatorcontrib><creatorcontrib>Chan, Kit Yu Karen</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><jtitle>Global change biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maboloc, Elizaldy A.</au><au>Chan, Kit Yu Karen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets</atitle><jtitle>Global change biology</jtitle><addtitle>Glob Chang Biol</addtitle><date>2021-07</date><risdate>2021</risdate><volume>27</volume><issue>14</issue><spage>3272</spage><epage>3281</epage><pages>3272-3281</pages><issn>1354-1013</issn><eissn>1365-2486</eissn><abstract>Multigenerational exposure is needed to assess the evolutionary potential of organisms in the rapidly changing seascape. Here, we investigate if there is a transgenerational effect of ocean acidification exposure on a calyptraeid gastropod such that long‐term exposure elevates offspring resilience. Larvae from wild type Crepidula onyx adults were reared from hatching until sexual maturity for over 36 months under three pH conditions (pH 7.3, 7.7, and 8.0). While the survivorship, growth, and respiration rate of F1 larvae were unaffected by acute ocean acidification (OA), long‐term and whole life cycle exposure significantly compromised adult survivorship, growth, and reproductive output of the slipper limpets. When kept under low pH throughout their life cycle, only 6% of the F1 slipper limpets survived pH 7.3 conditions after ~2.5 years and the number of larvae they released was ~10% of those released by the control. However, the F2 progeny from adults kept under the long‐term low pH condition hatched at a comparable size to those in medium and control pH conditions. More importantly, these F2 progeny from low pH adults outperformed F2 slipper limpets from control conditions; they had higher larval survivorship and growth, and reduced respiration rate across pH conditions, even at the extreme low pH of 7.0. The intragenerational negative consequences of OA during long‐term acclimation highlights potential carryover effects and ontogenetic shifts in stress vulnerability, especially prior to and during reproduction. Yet, the presence of a transgenerational effect implies that this slipper limpet, which has been widely introduced along the West Pacific coasts, has the potential to adapt to rapid acidification.
Slipper limpet larvae were previously shown to be resilient to ocean acidification (OA). However, whole life cycle exposure (from larvae to adult) to OA conditions reduced survivorship, growth, and reproductive output. OA exposure had a transgenerational effect such that larvae descend from OA exposed adults performed better under low pH conditions.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>33872435</pmid><doi>10.1111/gcb.15647</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-7775-4383</orcidid></addata></record> |
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subjects | Acclimation Acclimatization Acidification Adults anthropogenic stress carryover effect Control Exposure Growth Hatching Larvae Life cycle Life cycles Marine molluscs non‐indigenous species Ocean acidification Offspring Ontogeny pH control pH effects phenotypic plasticity Progeny Respiration Sexual maturity Survival Vulnerability |
title | Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets |
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