Abstract
BackgroundAnimal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection. Thermal behavior thus exemplifies a dynamic trait that requires non-trivial phenotypic summaries to appropriately capture the trait in response to a changing environment. To characterize the deterministic and plastic components of thermal responses, we developed a novel micro-droplet assay of nematode behavior that permits information-dense summaries of dynamic behavioral phenotypes as reaction norms in response to increasing temperature (thermal tolerance curves, TTC).ResultsWe found that C. elegans TTCs shift predictably with rearing conditions and developmental stage, with significant differences between distinct wildtype genetic backgrounds. Moreover, after screening TTCs for 58 C. elegans genetic mutant strains, we determined that genes affecting thermosensation, including cmk-1 and tax-4, potentially play important roles in the behavioral control of locomotion at high temperature, implicating neural decision-making in TTC shape rather than just generalized physiological limits. However, expression of the transient receptor potential ion channel TRPA-1 in the nervous system is not sufficient to rescue rearing-dependent plasticity in TTCs conferred by normal expression of this gene, indicating instead a role for intestinal signaling involving TRPA-1 in the adaptive plasticity of thermal performance.ConclusionsThese results implicate nervous system and non-nervous system contributions to behavior, in addition to basic cellular physiology, as key mediators of evolutionary responses to selection from temperature variation in nature.
Highlights
Animal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection
Caenorhabditis elegans swimming behavior as a thermal reaction norm We developed a micro-droplet assay of nematode worm swimming behavior that permits relatively high-throughput and information-dense quantification of individual locomotion in response to precise temperature manipulation
Worms are slightly more active when they experience a constant 25 °C compared to 21 °C or 23 °C
Summary
Animal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection. To characterize the deterministic and plastic components of thermal responses, we developed a novel micro-droplet assay of nematode behavior that permits information-dense summaries of dynamic behavioral phenotypes as reaction norms in response to increasing temperature (thermal tolerance curves, TTC). Behaviors are the primary way that animals interact with their environments and, in so doing, connect genetics and physiology with ecology. Natural selection favours those alleles of genes that allow animals to sense stimuli and react in ways that maximize fitness [1, 2]. In order to quantify the dynamic temperature-dependent behavior of Caenorhabditis nematode and to decipher its neuro-genetic control, we developed a novel assay to quantify locomotory behavior through a range of ecologically relevant temperature
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