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Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline
Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populat...
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Published in: | Molecular ecology 2018-05, Vol.27 (9), p.2243-2255 |
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creator | Campbell‐Staton, Shane C. Bare, Anna Losos, Jonathan B. Edwards, Scott V. Cheviron, Zachary A. |
description | Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CTmin), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co‐expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity‐limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.
see also the Perspective by Card et al. |
doi_str_mv | 10.1111/mec.14580 |
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see also the Perspective by Card et al.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.14580</identifier><identifier>PMID: 29633453</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Acclimation ; Acclimatization ; Adaptation ; Anolis ; Biological evolution ; Blood circulation ; Blood coagulation ; Blood levels ; Climate effects ; Clotting ; Coagulation ; Cold ; Cold tolerance ; Gene expression ; Heart rate ; Lactic acid ; Latitude ; Liver ; Metabolic rate ; metabolism ; Modules ; Natural populations ; Natural selection ; Oxygen ; Oxygen consumption ; Phenotypic plasticity ; Physiology ; Populations ; RNAseq ; Temperature tolerance ; Thermal stress ; thermal tolerance ; Variation</subject><ispartof>Molecular ecology, 2018-05, Vol.27 (9), p.2243-2255</ispartof><rights>2018 John Wiley & Sons Ltd</rights><rights>2018 John Wiley & Sons Ltd.</rights><rights>Copyright © 2018 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4540-894c6bc0c3c7679ac064db6fedd8d9c7129bcd9821ec81276b84ae5d96ca85643</citedby><cites>FETCH-LOGICAL-c4540-894c6bc0c3c7679ac064db6fedd8d9c7129bcd9821ec81276b84ae5d96ca85643</cites><orcidid>0000-0001-9778-7302</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29633453$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Campbell‐Staton, Shane C.</creatorcontrib><creatorcontrib>Bare, Anna</creatorcontrib><creatorcontrib>Losos, Jonathan B.</creatorcontrib><creatorcontrib>Edwards, Scott V.</creatorcontrib><creatorcontrib>Cheviron, Zachary A.</creatorcontrib><title>Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CTmin), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co‐expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity‐limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.
see also the Perspective by Card et al.</description><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Adaptation</subject><subject>Anolis</subject><subject>Biological evolution</subject><subject>Blood circulation</subject><subject>Blood coagulation</subject><subject>Blood levels</subject><subject>Climate effects</subject><subject>Clotting</subject><subject>Coagulation</subject><subject>Cold</subject><subject>Cold tolerance</subject><subject>Gene expression</subject><subject>Heart rate</subject><subject>Lactic acid</subject><subject>Latitude</subject><subject>Liver</subject><subject>Metabolic rate</subject><subject>metabolism</subject><subject>Modules</subject><subject>Natural populations</subject><subject>Natural selection</subject><subject>Oxygen</subject><subject>Oxygen consumption</subject><subject>Phenotypic plasticity</subject><subject>Physiology</subject><subject>Populations</subject><subject>RNAseq</subject><subject>Temperature tolerance</subject><subject>Thermal stress</subject><subject>thermal tolerance</subject><subject>Variation</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kU1P3DAQhq0KVLa0h_6ByhKXcgj4K058RCtKkUDtoZV6i5yxNxh57WAnRfn3eFnaAxK-zOWZZzzzIvSZkjNa3vnWwhkVdUveoRXlsq6YEn8O0IooySpKWn6EPuR8TwjlrK7foyOmJOei5iu0_Lxbsos-Dg60xzoYnOwwez3FtOA5GJtGF4ILQ8Zxgwcbh6THOwf4r05OTy4G7ELpGSfnnQ4Yojd4it4mHcBiDSnmjDUuRjfNxoUyBbwL9iM63Gif7aeXeox-f7v8tf5e3fy4ul5f3FQgakGqVgmQPRDg0MhGaSBSmF5urDGtUdBQpnowqmXUQktZI_tWaFsbJUG3tRT8GH3de8cUH2abp27rMljvdbBxzh0jjDflLA0p6Mkr9D7Oqfx4R_Eik1zsqNM99bxasptuTG6r09JR0u3y6Eoe3XMehf3yYpz7rTX_yX8BFOB8Dzw6b5e3Td3t5XqvfALKNpaH</recordid><startdate>201805</startdate><enddate>201805</enddate><creator>Campbell‐Staton, Shane C.</creator><creator>Bare, Anna</creator><creator>Losos, Jonathan B.</creator><creator>Edwards, Scott V.</creator><creator>Cheviron, Zachary A.</creator><general>Blackwell Publishing Ltd</general><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/0000-0001-9778-7302</orcidid></search><sort><creationdate>201805</creationdate><title>Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline</title><author>Campbell‐Staton, Shane C. ; Bare, Anna ; Losos, Jonathan B. ; Edwards, Scott V. ; Cheviron, Zachary A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4540-894c6bc0c3c7679ac064db6fedd8d9c7129bcd9821ec81276b84ae5d96ca85643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Adaptation</topic><topic>Anolis</topic><topic>Biological evolution</topic><topic>Blood circulation</topic><topic>Blood coagulation</topic><topic>Blood levels</topic><topic>Climate effects</topic><topic>Clotting</topic><topic>Coagulation</topic><topic>Cold</topic><topic>Cold tolerance</topic><topic>Gene expression</topic><topic>Heart rate</topic><topic>Lactic acid</topic><topic>Latitude</topic><topic>Liver</topic><topic>Metabolic rate</topic><topic>metabolism</topic><topic>Modules</topic><topic>Natural populations</topic><topic>Natural selection</topic><topic>Oxygen</topic><topic>Oxygen consumption</topic><topic>Phenotypic plasticity</topic><topic>Physiology</topic><topic>Populations</topic><topic>RNAseq</topic><topic>Temperature tolerance</topic><topic>Thermal stress</topic><topic>thermal tolerance</topic><topic>Variation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Campbell‐Staton, Shane C.</creatorcontrib><creatorcontrib>Bare, Anna</creatorcontrib><creatorcontrib>Losos, Jonathan B.</creatorcontrib><creatorcontrib>Edwards, Scott V.</creatorcontrib><creatorcontrib>Cheviron, Zachary A.</creatorcontrib><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>Campbell‐Staton, Shane C.</au><au>Bare, Anna</au><au>Losos, Jonathan B.</au><au>Edwards, Scott V.</au><au>Cheviron, Zachary A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2018-05</date><risdate>2018</risdate><volume>27</volume><issue>9</issue><spage>2243</spage><epage>2255</epage><pages>2243-2255</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CTmin), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co‐expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity‐limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.
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subjects | Acclimation Acclimatization Adaptation Anolis Biological evolution Blood circulation Blood coagulation Blood levels Climate effects Clotting Coagulation Cold Cold tolerance Gene expression Heart rate Lactic acid Latitude Liver Metabolic rate metabolism Modules Natural populations Natural selection Oxygen Oxygen consumption Phenotypic plasticity Physiology Populations RNAseq Temperature tolerance Thermal stress thermal tolerance Variation |
title | Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline |
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