Assessing hybrid vigour using the thermal sensitivity of physiological trade-offs in tiger salamanders
Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to th...
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creator | Burger, Isabella J. Carter, Evin T. Magner, Lexie M. Muñoz, Martha M. Sears, Michael W. Fitzpatrick, Benjamin M. Riddell, Eric A. |
description | Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines. In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water-gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μL VO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance. We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss. These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species- or lineage-wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance. |
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Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines. In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water-gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μL VO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance. We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss. These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species- or lineage-wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance.</description><identifier>ISSN: 0269-8463</identifier><identifier>EISSN: 1365-2435</identifier><language>eng</language><publisher>United States: British Ecological Society; Wiley</publisher><subject>BASIC BIOLOGICAL SCIENCES ; gas exchange ; genotype ; hybridization ; metabolism ; respiration efficiency ; salamander ; trade-offs ; water loss</subject><ispartof>Functional ecology, 2023-11, Vol.38 (1)</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>000000030153578X ; 0000000241434791 ; 0000000242294911 ; 0000000217327662 ; 0000000182972396 ; 0000000285568716</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885</link.rule.ids><backlink>$$Uhttps://www.osti.gov/servlets/purl/2301646$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Burger, Isabella J.</creatorcontrib><creatorcontrib>Carter, Evin T.</creatorcontrib><creatorcontrib>Magner, Lexie M.</creatorcontrib><creatorcontrib>Muñoz, Martha M.</creatorcontrib><creatorcontrib>Sears, Michael W.</creatorcontrib><creatorcontrib>Fitzpatrick, Benjamin M.</creatorcontrib><creatorcontrib>Riddell, Eric A.</creatorcontrib><creatorcontrib>Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)</creatorcontrib><title>Assessing hybrid vigour using the thermal sensitivity of physiological trade-offs in tiger salamanders</title><title>Functional ecology</title><description>Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines. In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water-gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μL VO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance. We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss. These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species- or lineage-wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance.</description><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>gas exchange</subject><subject>genotype</subject><subject>hybridization</subject><subject>metabolism</subject><subject>respiration efficiency</subject><subject>salamander</subject><subject>trade-offs</subject><subject>water loss</subject><issn>0269-8463</issn><issn>1365-2435</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqNjssKwjAQRYMoWB__MLgvxPSBLkUUP8C9xHTSjrSJZGKhf28VP8DF5cK5Z3EnItlmZZGqPCumIpGq3Ke7vMzmYsH8kFLuC6USYQ_MyEyuhma4B6qgp9q_Ary-LDb4Seh0C4yOKVJPcQBv4dkMTL71NZlxjEFXmHprGchBpBoDsG51p12FgVdiZnXLuP71UmzOp-vxknqOdGNDEU1jvHNo4k1lcluOV_-S3g4XSZE</recordid><startdate>20231110</startdate><enddate>20231110</enddate><creator>Burger, Isabella J.</creator><creator>Carter, Evin T.</creator><creator>Magner, Lexie M.</creator><creator>Muñoz, Martha M.</creator><creator>Sears, Michael W.</creator><creator>Fitzpatrick, Benjamin M.</creator><creator>Riddell, Eric A.</creator><general>British Ecological Society; Wiley</general><scope>OIOZB</scope><scope>OTOTI</scope><orcidid>https://orcid.org/000000030153578X</orcidid><orcidid>https://orcid.org/0000000241434791</orcidid><orcidid>https://orcid.org/0000000242294911</orcidid><orcidid>https://orcid.org/0000000217327662</orcidid><orcidid>https://orcid.org/0000000182972396</orcidid><orcidid>https://orcid.org/0000000285568716</orcidid></search><sort><creationdate>20231110</creationdate><title>Assessing hybrid vigour using the thermal sensitivity of physiological trade-offs in tiger salamanders</title><author>Burger, Isabella J. ; Carter, Evin T. ; Magner, Lexie M. ; Muñoz, Martha M. ; Sears, Michael W. ; Fitzpatrick, Benjamin M. ; Riddell, Eric A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-osti_scitechconnect_23016463</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>gas exchange</topic><topic>genotype</topic><topic>hybridization</topic><topic>metabolism</topic><topic>respiration efficiency</topic><topic>salamander</topic><topic>trade-offs</topic><topic>water loss</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Burger, Isabella J.</creatorcontrib><creatorcontrib>Carter, Evin T.</creatorcontrib><creatorcontrib>Magner, Lexie M.</creatorcontrib><creatorcontrib>Muñoz, Martha M.</creatorcontrib><creatorcontrib>Sears, Michael W.</creatorcontrib><creatorcontrib>Fitzpatrick, Benjamin M.</creatorcontrib><creatorcontrib>Riddell, Eric A.</creatorcontrib><creatorcontrib>Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)</creatorcontrib><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><jtitle>Functional ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Burger, Isabella J.</au><au>Carter, Evin T.</au><au>Magner, Lexie M.</au><au>Muñoz, Martha M.</au><au>Sears, Michael W.</au><au>Fitzpatrick, Benjamin M.</au><au>Riddell, Eric A.</au><aucorp>Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Assessing hybrid vigour using the thermal sensitivity of physiological trade-offs in tiger salamanders</atitle><jtitle>Functional ecology</jtitle><date>2023-11-10</date><risdate>2023</risdate><volume>38</volume><issue>1</issue><issn>0269-8463</issn><eissn>1365-2435</eissn><abstract>Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines. In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water-gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μL VO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance. We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss. These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. 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subjects | BASIC BIOLOGICAL SCIENCES gas exchange genotype hybridization metabolism respiration efficiency salamander trade-offs water loss |
title | Assessing hybrid vigour using the thermal sensitivity of physiological trade-offs in tiger salamanders |
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