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Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves

Thermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its dynamic dependence on environmental stimuli p...

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Autores principales: Stegeman, Gregory W., Baird, Scott E., Ryu, William S., Cutter, Asher D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6643873/
https://www.ncbi.nlm.nih.gov/pubmed/31048400
http://dx.doi.org/10.1534/g3.119.400043
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author Stegeman, Gregory W.
Baird, Scott E.
Ryu, William S.
Cutter, Asher D.
author_facet Stegeman, Gregory W.
Baird, Scott E.
Ryu, William S.
Cutter, Asher D.
author_sort Stegeman, Gregory W.
collection PubMed
description Thermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its dynamic dependence on environmental stimuli presenting a challenge for analysis and for understanding the genomic architecture of heritable variation. Here we characterize behavioral reaction norms as thermal performance curves for the nematode Caenorhabditis briggsae, using a collection of 23 wild isolate genotypes and 153 recombinant inbred lines to quantify the extent of genetic and plastic variation in locomotory behavior to temperature changes. By reducing the dimensionality of the multivariate phenotypic response with a function-valued trait framework, we identified genetically distinct behavioral modules that contribute to the heritable variation in the emergent overall behavioral thermal performance curve. Quantitative trait locus mapping isolated regions on Chromosome II associated with locomotory activity at benign temperatures and Chromosome V loci related to distinct aspects of sensitivity to high temperatures, with each quantitative trait locus explaining up to 28% of trait variation. These findings highlight how behavioral responses to environmental inputs as thermal reaction norms can evolve through independent changes to genetically distinct modular components of such complex phenotypes.
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spelling pubmed-66438732019-07-25 Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves Stegeman, Gregory W. Baird, Scott E. Ryu, William S. Cutter, Asher D. G3 (Bethesda) Investigations Thermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its dynamic dependence on environmental stimuli presenting a challenge for analysis and for understanding the genomic architecture of heritable variation. Here we characterize behavioral reaction norms as thermal performance curves for the nematode Caenorhabditis briggsae, using a collection of 23 wild isolate genotypes and 153 recombinant inbred lines to quantify the extent of genetic and plastic variation in locomotory behavior to temperature changes. By reducing the dimensionality of the multivariate phenotypic response with a function-valued trait framework, we identified genetically distinct behavioral modules that contribute to the heritable variation in the emergent overall behavioral thermal performance curve. Quantitative trait locus mapping isolated regions on Chromosome II associated with locomotory activity at benign temperatures and Chromosome V loci related to distinct aspects of sensitivity to high temperatures, with each quantitative trait locus explaining up to 28% of trait variation. These findings highlight how behavioral responses to environmental inputs as thermal reaction norms can evolve through independent changes to genetically distinct modular components of such complex phenotypes. Genetics Society of America 2019-05-02 /pmc/articles/PMC6643873/ /pubmed/31048400 http://dx.doi.org/10.1534/g3.119.400043 Text en Copyright © 2019 Stegeman et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigations
Stegeman, Gregory W.
Baird, Scott E.
Ryu, William S.
Cutter, Asher D.
Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title_full Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title_fullStr Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title_full_unstemmed Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title_short Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves
title_sort genetically distinct behavioral modules underlie natural variation in thermal performance curves
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6643873/
https://www.ncbi.nlm.nih.gov/pubmed/31048400
http://dx.doi.org/10.1534/g3.119.400043
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