Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate
An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G) and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alter...
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Veröffentlicht in: | The Journal of animal ecology 2020-08, Vol.89 (8), p.1883-1894 |
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creator | Palacios, Maria G. Gangloff, Eric J. Reding, Dawn M. Bronikowski, Anne M. Richardson, David |
description | An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G) and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alterations in temperature regimes have been implicated in emergent disease outbreaks, making it a critical environmental factor to study in the context of immune phenotype determinants of wild animals.
We assessed the relative influences of environmental temperature, genetic background and their interaction on first‐year development of innate and adaptive immune defences of captive‐born garter snakes Thamnophis elegans using a reciprocal transplant laboratory experiment. We used a full‐factorial design with snakes from two divergent life‐history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime—that is, warmer and cooler—of each habitat.
Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune‐component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast‐ and the slow‐paced life‐history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development.
Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune‐component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.
Understanding the relative contribution |
doi_str_mv | 10.1111/1365-2656.13271 |
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We assessed the relative influences of environmental temperature, genetic background and their interaction on first‐year development of innate and adaptive immune defences of captive‐born garter snakes Thamnophis elegans using a reciprocal transplant laboratory experiment. We used a full‐factorial design with snakes from two divergent life‐history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime—that is, warmer and cooler—of each habitat.
Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune‐component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast‐ and the slow‐paced life‐history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development.
Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune‐component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.
Understanding the relative contribution of environmental and genetic factors in shaping immune defenses is critical in the context of rapid global environmental changes. This experimental study in garter snakes contributes to this understudied aspect of vertebrate ecoimmunology by deepening our understanding on immunological flexibility in wildlife while contemplating the complexity of the vertebrate immune system.</description><identifier>ISSN: 0021-8790</identifier><identifier>EISSN: 1365-2656</identifier><identifier>DOI: 10.1111/1365-2656.13271</identifier><identifier>PMID: 32472604</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>adaptive immunity ; Animals ; Colubridae ; Context ; Divergence ; ecoimmunology ; Ecosystem ; Ecotypes ; Environmental changes ; Environmental effects ; Environmental factors ; Factorial design ; Food consumption ; Genetic Background ; Growth and Development ; Immune response ; Immune system ; Immunology ; innate immunity ; life history ; Mimicry ; Ontogeny ; Parameters ; Phenotypes ; phenotypic plasticity ; Resource allocation ; Snakes ; Temperature ; Thamnophis ; Thermal environments ; Vertebrates ; Wild animals</subject><ispartof>The Journal of animal ecology, 2020-08, Vol.89 (8), p.1883-1894</ispartof><rights>2020 British Ecological Society</rights><rights>2020 British Ecological Society.</rights><rights>Journal of Animal Ecology © 2020 British Ecological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4131-3c9d8667b2cbff72ce95ccfcc6060abad60090d6904681f5da145c71b9c07bd53</citedby><cites>FETCH-LOGICAL-c4131-3c9d8667b2cbff72ce95ccfcc6060abad60090d6904681f5da145c71b9c07bd53</cites><orcidid>0000-0003-3206-5581 ; 0000-0001-6432-298X</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%2F1365-2656.13271$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1365-2656.13271$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27903,27904,45553,45554,46387,46811</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32472604$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Richardson, David</contributor><creatorcontrib>Palacios, Maria G.</creatorcontrib><creatorcontrib>Gangloff, Eric J.</creatorcontrib><creatorcontrib>Reding, Dawn M.</creatorcontrib><creatorcontrib>Bronikowski, Anne M.</creatorcontrib><creatorcontrib>Richardson, David</creatorcontrib><title>Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate</title><title>The Journal of animal ecology</title><addtitle>J Anim Ecol</addtitle><description>An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G) and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alterations in temperature regimes have been implicated in emergent disease outbreaks, making it a critical environmental factor to study in the context of immune phenotype determinants of wild animals.
We assessed the relative influences of environmental temperature, genetic background and their interaction on first‐year development of innate and adaptive immune defences of captive‐born garter snakes Thamnophis elegans using a reciprocal transplant laboratory experiment. We used a full‐factorial design with snakes from two divergent life‐history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime—that is, warmer and cooler—of each habitat.
Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune‐component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast‐ and the slow‐paced life‐history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development.
Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune‐component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.
Understanding the relative contribution of environmental and genetic factors in shaping immune defenses is critical in the context of rapid global environmental changes. This experimental study in garter snakes contributes to this understudied aspect of vertebrate ecoimmunology by deepening our understanding on immunological flexibility in wildlife while contemplating the complexity of the vertebrate immune system.</description><subject>adaptive immunity</subject><subject>Animals</subject><subject>Colubridae</subject><subject>Context</subject><subject>Divergence</subject><subject>ecoimmunology</subject><subject>Ecosystem</subject><subject>Ecotypes</subject><subject>Environmental changes</subject><subject>Environmental effects</subject><subject>Environmental factors</subject><subject>Factorial design</subject><subject>Food consumption</subject><subject>Genetic Background</subject><subject>Growth and Development</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunology</subject><subject>innate immunity</subject><subject>life history</subject><subject>Mimicry</subject><subject>Ontogeny</subject><subject>Parameters</subject><subject>Phenotypes</subject><subject>phenotypic plasticity</subject><subject>Resource allocation</subject><subject>Snakes</subject><subject>Temperature</subject><subject>Thamnophis</subject><subject>Thermal environments</subject><subject>Vertebrates</subject><subject>Wild animals</subject><issn>0021-8790</issn><issn>1365-2656</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkTFvFDEQhS0EIkegpkOWaNJsMrZ37dsyikIARaQJteW1x4fDrn3Yu0H3P_KD8eVCChpGsmZkfe_NSI-Q9wxOWa0zJmTXcNnJUya4Yi_I6vnnJVkBcNasVQ9H5E0pdwCgOIjX5EjwVnEJ7Yo8XGHEOVg6GPtzk9MSHTX1zT8wT2akGO9DTnHCOFMXvMdcp2DGcUdD9OOC0eIepinOaYNxR5OnYZqWiNSmaZti5Qt1Sw5xQ9HkKhyDx6queyjaOT2uqhfcY55xyGbGt-SVN2PBd0_9mHz_dHl78bm5vrn6cnF-3diWCdYI27u1lGrgdvBecYt9Z623VoIEMxgnAXpwsodWrpnvnGFtZxUbegtqcJ04JicH321OvxYss55CsTiOJmJaiuYtrFnPuWAV_fgPepeWHOt1lRIgJFNSVersQNmcSsno9TaHyeSdZqD3gel9PHofj34MrCo-PPkuw4Tumf-bUAXkAfgdRtz9z09_Pf92eXD-A97Vox8</recordid><startdate>202008</startdate><enddate>202008</enddate><creator>Palacios, Maria G.</creator><creator>Gangloff, Eric J.</creator><creator>Reding, Dawn M.</creator><creator>Bronikowski, Anne M.</creator><creator>Richardson, David</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>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3206-5581</orcidid><orcidid>https://orcid.org/0000-0001-6432-298X</orcidid></search><sort><creationdate>202008</creationdate><title>Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate</title><author>Palacios, Maria G. ; Gangloff, Eric J. ; Reding, Dawn M. ; Bronikowski, Anne M. ; Richardson, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4131-3c9d8667b2cbff72ce95ccfcc6060abad60090d6904681f5da145c71b9c07bd53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>adaptive immunity</topic><topic>Animals</topic><topic>Colubridae</topic><topic>Context</topic><topic>Divergence</topic><topic>ecoimmunology</topic><topic>Ecosystem</topic><topic>Ecotypes</topic><topic>Environmental changes</topic><topic>Environmental effects</topic><topic>Environmental factors</topic><topic>Factorial design</topic><topic>Food consumption</topic><topic>Genetic Background</topic><topic>Growth and Development</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunology</topic><topic>innate immunity</topic><topic>life history</topic><topic>Mimicry</topic><topic>Ontogeny</topic><topic>Parameters</topic><topic>Phenotypes</topic><topic>phenotypic plasticity</topic><topic>Resource allocation</topic><topic>Snakes</topic><topic>Temperature</topic><topic>Thamnophis</topic><topic>Thermal environments</topic><topic>Vertebrates</topic><topic>Wild animals</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Palacios, Maria G.</creatorcontrib><creatorcontrib>Gangloff, Eric J.</creatorcontrib><creatorcontrib>Reding, Dawn M.</creatorcontrib><creatorcontrib>Bronikowski, Anne M.</creatorcontrib><creatorcontrib>Richardson, David</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</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>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of animal ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Palacios, Maria G.</au><au>Gangloff, Eric J.</au><au>Reding, Dawn M.</au><au>Bronikowski, Anne M.</au><au>Richardson, David</au><au>Richardson, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate</atitle><jtitle>The Journal of animal ecology</jtitle><addtitle>J Anim Ecol</addtitle><date>2020-08</date><risdate>2020</risdate><volume>89</volume><issue>8</issue><spage>1883</spage><epage>1894</epage><pages>1883-1894</pages><issn>0021-8790</issn><eissn>1365-2656</eissn><abstract>An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G) and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alterations in temperature regimes have been implicated in emergent disease outbreaks, making it a critical environmental factor to study in the context of immune phenotype determinants of wild animals.
We assessed the relative influences of environmental temperature, genetic background and their interaction on first‐year development of innate and adaptive immune defences of captive‐born garter snakes Thamnophis elegans using a reciprocal transplant laboratory experiment. We used a full‐factorial design with snakes from two divergent life‐history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime—that is, warmer and cooler—of each habitat.
Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune‐component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast‐ and the slow‐paced life‐history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development.
Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune‐component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.
Understanding the relative contribution of environmental and genetic factors in shaping immune defenses is critical in the context of rapid global environmental changes. This experimental study in garter snakes contributes to this understudied aspect of vertebrate ecoimmunology by deepening our understanding on immunological flexibility in wildlife while contemplating the complexity of the vertebrate immune system.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32472604</pmid><doi>10.1111/1365-2656.13271</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-3206-5581</orcidid><orcidid>https://orcid.org/0000-0001-6432-298X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | adaptive immunity Animals Colubridae Context Divergence ecoimmunology Ecosystem Ecotypes Environmental changes Environmental effects Environmental factors Factorial design Food consumption Genetic Background Growth and Development Immune response Immune system Immunology innate immunity life history Mimicry Ontogeny Parameters Phenotypes phenotypic plasticity Resource allocation Snakes Temperature Thamnophis Thermal environments Vertebrates Wild animals |
title | Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate |
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