Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California

Accurately predicting the effects of future warming on aquatic ectotherms requires an understanding how thermal history, including average temperature and variation, affects populations of the same species. However, many laboratory studies simplify the thermal environment to focus on specific organi...

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Main Authors: Emily E. King, Jonathon H. Stillman
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2022.990390/full
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author Emily E. King
Jonathon H. Stillman
Jonathon H. Stillman
author_facet Emily E. King
Jonathon H. Stillman
Jonathon H. Stillman
author_sort Emily E. King
collection DOAJ
description Accurately predicting the effects of future warming on aquatic ectotherms requires an understanding how thermal history, including average temperature and variation, affects populations of the same species. However, many laboratory studies simplify the thermal environment to focus on specific organismal responses and sacrifice environmental realism. Here, we paired laboratory-based transcriptomic RNA-seq analysis to identify thermally responsive genes with NanoString analysis of a subset of those genes to characterize natural field-based variation in thermal physiology among populations. We tested gene expression responses of three populations of field-acclimatized larval caddisflies (Dicosmoecus gilvipes) from streams in different eco-regions (mountain, valley, and coast) following exposure to current and future summertime temperatures. We hypothesized that distinct thermal histories across eco-regions could differentiate populations at baseline “control” levels of gene expression, as well as gene expression changes in response to daily warming and heat shock. Population-specific patterns of gene expression were apparent under the control and daily warming conditions suggesting that local acclimatization or local adaptation may differentiate populations, while responses to extreme temperatures were similar across populations, indicating that response to thermal stress is canalized. Underlying gene co-expression patterns in the daily warming and heat shock treatments were different, demonstrating the distinct physiological mechanisms involved with thermal acclimatization and response to thermal stress. These results highlight the importance and limitations of studies of the thermal biology of wild-caught organisms in their natural environment, and provide an important resource for researchers of caddisflies and aquatic insects in general.
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spelling doaj.art-727e1fa3748c41a2a6ee69fef851b5712022-12-22T02:25:33ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-10-011310.3389/fphys.2022.990390990390Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in CaliforniaEmily E. King0Jonathon H. Stillman1Jonathon H. Stillman2Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Biology, San Francisco State University, San Francisco, CA, United StatesAccurately predicting the effects of future warming on aquatic ectotherms requires an understanding how thermal history, including average temperature and variation, affects populations of the same species. However, many laboratory studies simplify the thermal environment to focus on specific organismal responses and sacrifice environmental realism. Here, we paired laboratory-based transcriptomic RNA-seq analysis to identify thermally responsive genes with NanoString analysis of a subset of those genes to characterize natural field-based variation in thermal physiology among populations. We tested gene expression responses of three populations of field-acclimatized larval caddisflies (Dicosmoecus gilvipes) from streams in different eco-regions (mountain, valley, and coast) following exposure to current and future summertime temperatures. We hypothesized that distinct thermal histories across eco-regions could differentiate populations at baseline “control” levels of gene expression, as well as gene expression changes in response to daily warming and heat shock. Population-specific patterns of gene expression were apparent under the control and daily warming conditions suggesting that local acclimatization or local adaptation may differentiate populations, while responses to extreme temperatures were similar across populations, indicating that response to thermal stress is canalized. Underlying gene co-expression patterns in the daily warming and heat shock treatments were different, demonstrating the distinct physiological mechanisms involved with thermal acclimatization and response to thermal stress. These results highlight the importance and limitations of studies of the thermal biology of wild-caught organisms in their natural environment, and provide an important resource for researchers of caddisflies and aquatic insects in general.https://www.frontiersin.org/articles/10.3389/fphys.2022.990390/fullgene expressioncaddisflythermalectothermwarminglocal adaptation
spellingShingle Emily E. King
Jonathon H. Stillman
Jonathon H. Stillman
Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
Frontiers in Physiology
gene expression
caddisfly
thermal
ectotherm
warming
local adaptation
title Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
title_full Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
title_fullStr Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
title_full_unstemmed Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
title_short Mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of Dicosmoecus gilvipes in California
title_sort mild temperatures differentiate while extreme temperatures unify gene expression profiles among populations of dicosmoecus gilvipes in california
topic gene expression
caddisfly
thermal
ectotherm
warming
local adaptation
url https://www.frontiersin.org/articles/10.3389/fphys.2022.990390/full
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