Toxicity and population structure of the Rough‐Skinned Newt (Taricha granulosa) outside the range of an arms race with resistant predators

Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from...

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Veröffentlicht in:Ecology and evolution 2016-05, Vol.6 (9), p.2714-2724
Hauptverfasser: Hague, Michael T.J., Avila, Leleña A., Hanifin, Charles T., Snedden, W. Andrew, Stokes, Amber N., Brodie, Edmund D.
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container_end_page 2724
container_issue 9
container_start_page 2714
container_title Ecology and evolution
container_volume 6
creator Hague, Michael T.J.
Avila, Leleña A.
Hanifin, Charles T.
Snedden, W. Andrew
Stokes, Amber N.
Brodie, Edmund D.
Brodie, Edmund D.
description Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. We examine phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt (Taricha granulosa) in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake (Thamnophis sirtalis). In sympatry, geographic patterns of phenotypic exaggeration in toxicity and toxin‐resistance are closely correlated in prey and predator, implying that reciprocal selection drives phenotypic variation in coevolutionary traits. Therefore, in allopatry with TTX‐resistant predators, we expect to find uniformly low levels of newt toxicity. We characterized TTX toxicity in northwestern North America, including the Alaskan panhandle where Ta. granulosa occur in allopatry with Th. sirtalis. First, we used microsatellite markers to estimate population genetic structure and determine if any phenotypic variation in toxicity might be explained by historical divergence. We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa. We examined phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. These results suggest that forces o
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Andrew ; Stokes, Amber N. ; Brodie, Edmund D. ; Brodie, Edmund D.</creator><creatorcontrib>Hague, Michael T.J. ; Avila, Leleña A. ; Hanifin, Charles T. ; Snedden, W. Andrew ; Stokes, Amber N. ; Brodie, Edmund D. ; Brodie, Edmund D.</creatorcontrib><description>Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. We examine phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt (Taricha granulosa) in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake (Thamnophis sirtalis). In sympatry, geographic patterns of phenotypic exaggeration in toxicity and toxin‐resistance are closely correlated in prey and predator, implying that reciprocal selection drives phenotypic variation in coevolutionary traits. Therefore, in allopatry with TTX‐resistant predators, we expect to find uniformly low levels of newt toxicity. We characterized TTX toxicity in northwestern North America, including the Alaskan panhandle where Ta. granulosa occur in allopatry with Th. sirtalis. First, we used microsatellite markers to estimate population genetic structure and determine if any phenotypic variation in toxicity might be explained by historical divergence. We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa. We examined phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. These results suggest that forces other than reciprocal selection with resistant predators contribute to geographic patterns of variation in newt toxicity.</description><identifier>ISSN: 2045-7758</identifier><identifier>EISSN: 2045-7758</identifier><identifier>DOI: 10.1002/ece3.2068</identifier><identifier>PMID: 27066249</identifier><language>eng</language><publisher>England: John Wiley &amp; Sons, Inc</publisher><subject>Adaptation ; Allopatric populations ; Allopatry ; Arms race ; coevolution ; Divergence ; Evolution &amp; development ; Fitness ; Genetic markers ; Genetic structure ; Geography ; Heterogeneity ; Islands ; Levels ; Microsatellites ; Original Research ; Phenotypic variations ; Physiology ; Pleistocene ; Population ; Population genetics ; Population structure ; Populations ; Predators ; Prey ; Range extension ; Reproductive fitness ; Salamandridae ; Skin ; Snakes ; Spatial heterogeneity ; Sympatry ; Taricha granulosa ; Tetrodotoxin ; Thamnophis sirtalis ; Toxicity ; Toxins</subject><ispartof>Ecology and evolution, 2016-05, Vol.6 (9), p.2714-2724</ispartof><rights>2016 The Authors. published by John Wiley &amp; Sons Ltd.</rights><rights>2016. 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Andrew</creatorcontrib><creatorcontrib>Stokes, Amber N.</creatorcontrib><creatorcontrib>Brodie, Edmund D.</creatorcontrib><creatorcontrib>Brodie, Edmund D.</creatorcontrib><title>Toxicity and population structure of the Rough‐Skinned Newt (Taricha granulosa) outside the range of an arms race with resistant predators</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. 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We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa. We examined phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake. 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Andrew</au><au>Stokes, Amber N.</au><au>Brodie, Edmund D.</au><au>Brodie, Edmund D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Toxicity and population structure of the Rough‐Skinned Newt (Taricha granulosa) outside the range of an arms race with resistant predators</atitle><jtitle>Ecology and evolution</jtitle><addtitle>Ecol Evol</addtitle><date>2016-05</date><risdate>2016</risdate><volume>6</volume><issue>9</issue><spage>2714</spage><epage>2724</epage><pages>2714-2724</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. We examine phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt (Taricha granulosa) in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake (Thamnophis sirtalis). In sympatry, geographic patterns of phenotypic exaggeration in toxicity and toxin‐resistance are closely correlated in prey and predator, implying that reciprocal selection drives phenotypic variation in coevolutionary traits. Therefore, in allopatry with TTX‐resistant predators, we expect to find uniformly low levels of newt toxicity. We characterized TTX toxicity in northwestern North America, including the Alaskan panhandle where Ta. granulosa occur in allopatry with Th. sirtalis. First, we used microsatellite markers to estimate population genetic structure and determine if any phenotypic variation in toxicity might be explained by historical divergence. We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa. We examined phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. These results suggest that forces other than reciprocal selection with resistant predators contribute to geographic patterns of variation in newt toxicity.</abstract><cop>England</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>27066249</pmid><doi>10.1002/ece3.2068</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record>
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subjects Adaptation
Allopatric populations
Allopatry
Arms race
coevolution
Divergence
Evolution & development
Fitness
Genetic markers
Genetic structure
Geography
Heterogeneity
Islands
Levels
Microsatellites
Original Research
Phenotypic variations
Physiology
Pleistocene
Population
Population genetics
Population structure
Populations
Predators
Prey
Range extension
Reproductive fitness
Salamandridae
Skin
Snakes
Spatial heterogeneity
Sympatry
Taricha granulosa
Tetrodotoxin
Thamnophis sirtalis
Toxicity
Toxins
title Toxicity and population structure of the Rough‐Skinned Newt (Taricha granulosa) outside the range of an arms race with resistant predators
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