Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

John Stanton-Geddes; Andrew Nguyen; Lacy Chick; James Vincent; Mahesh Vangala; Robert R. Dunn; Aaron M. Ellison; Nate Sanders; Nicholas J. Gotelli; Sara Helms Cahan

doi:10.1186/s12864-016-2466-z

Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

John Stanton-Geddes, Andrew Nguyen, Lacy Chick, James Vincent, Mahesh Vangala, Robert R. Dunn, Aaron M. Ellison, Nate Sanders, Nicholas J. Gotelli, Sara Helms Cahan

11 Citations (Scopus)

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Abstract

Background: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism's transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. Results: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. Conclusions: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.

Original language	English
Article number	171
Journal	BMC Genomics
Volume	17
Number of pages	15
ISSN	1471-2164
DOIs	https://doi.org/10.1186/s12864-016-2466-z
Publication status	Published - 2 Mar 2016

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Cite this

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title = "Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species",

abstract = "Background: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism's transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. Results: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. Conclusions: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.",

author = "John Stanton-Geddes and Andrew Nguyen and Lacy Chick and James Vincent and Mahesh Vangala and Dunn, {Robert R.} and Ellison, {Aaron M.} and Nate Sanders and Gotelli, {Nicholas J.} and Cahan, {Sara Helms}",

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doi = "10.1186/s12864-016-2466-z",

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T1 - Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

AU - Stanton-Geddes, John

AU - Nguyen, Andrew

AU - Chick, Lacy

AU - Vincent, James

AU - Vangala, Mahesh

AU - Dunn, Robert R.

AU - Ellison, Aaron M.

AU - Sanders, Nate

AU - Gotelli, Nicholas J.

AU - Cahan, Sara Helms

PY - 2016/3/2

Y1 - 2016/3/2

N2 - Background: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism's transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. Results: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. Conclusions: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.

AB - Background: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism's transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. Results: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. Conclusions: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.

U2 - 10.1186/s12864-016-2466-z

DO - 10.1186/s12864-016-2466-z

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SN - 1471-2164

VL - 17

JO - BMC Genomics

JF - BMC Genomics

M1 - 171

ER -

Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

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