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Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves.

ABSTRACT: 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.

SUBMITTER: Stegeman GW

PROVIDER: S-EPMC6643873 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves.

Stegeman Gregory W GW Baird Scott E SE Ryu William S WS Cutter Asher D AD

G3 (Bethesda, Md.) 20190709 7

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 ...[more]

PMID: 31048400

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Project description:Understanding links between thermal performance and environmental variation is necessary to predict organismal responses to climate change, and remains an ongoing challenge for ectotherms with complex life cycles. Distinct life stages can differ in thermal sensitivity, experience different environmental conditions as development unfolds, and, because stages are by nature interdependent, environmental effects can carry over from one stage to affect performance at others. Thermal performance may therefore respond to carryover effects of prior thermal environments, yet detailed insights into the nature, strength, and direction of those responses are still lacking. Here, in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics, we explore the effects of prior thermal environments at fertilization and embryogenesis on thermal performance curves at the end of planktonic development. We factorially manipulate temperatures at fertilization and embryogenesis, then, for each combination of prior temperatures, measure thermal performance curves for survival of planktonic development (end of the larval stage) throughout the performance range. By combining generalized linear mixed modeling with parametric bootstrapping, we formally estimate and compare curve descriptors (thermal optima, limits, and breadth) among prior environments, and reveal carryover effects of temperature at embryogenesis, but not fertilization, on thermal optima at completion of development. Specifically, thermal optima shifted to track temperature during embryogenesis, while thermal limits and breadth remained unchanged. Our results argue that key aspects of thermal performance are shaped by prior thermal environment in early life, warranting further investigation of the possible mechanisms underpinning that response, and closer consideration of thermal carryover effects when predicting organismal responses to climate change.

Dataset Information

Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves.

Publications

Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves.

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