Neuro-genetic plasticity of Caenorhabditis elegans behavioral thermal tolerance

Abstract

Background Animal 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). Results We 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. Conclusions These 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. Electronic supplementary material The online version of this article (10.1186/s12868-019-0510-z) contains supplementary material, which is available to authorized users.

Genetically distinct behavioral modules underlie natural variation in thermal performance curves

“…We hypothesized that rearing temperature would differentially affect thermal performance of swimming behavior of distinct genotypes, motivated by prior studies that demonstrated temperature-dependent trait differences among phylogeographic groups of C. briggsae (PRASAD et al 2011;STEGEMAN et al 2013). We therefore quantified natural genetic variation and environmental plasticity in locomotion behavior in C. briggsae by assaying thermal performance with a liquid micro-droplet experimental paradigm described previously (STEGEMAN et al 2019).…”

“…Analysis of behavioral reaction norms in Caenorhabditis elegans demonstrated a neural 'decision-making' contribution to temperature-dependent locomotory responses using the same experimental paradigm as we here investigate in its congener C. briggsae (STEGEMAN et al 2019). C. briggsae may provide an even more powerful animal model system to investigate natural genetic variation in temperature-dependent behavioral reaction norms.…”

“…We quantified nematode locomotory behavior as a function of changes in temperature using the liquid micro-droplet experimental paradigm that we developed previously (STEGEMAN et al 2019). In brief, we recorded video and quantified the swimming behavior of individual worms placed into 1.8µL droplets arranged in an array of 18 droplets on a glass slide as we manipulated temperature with custom hardware (STEGEMAN et al 2019).…”

“…We quantified nematode locomotory behavior as a function of changes in temperature using the liquid micro-droplet experimental paradigm that we developed previously (STEGEMAN et al 2019). In brief, we recorded video and quantified the swimming behavior of individual worms placed into 1.8µL droplets arranged in an array of 18 droplets on a glass slide as we manipulated temperature with custom hardware (STEGEMAN et al 2019). Image capture and processing of swimming worms was performed with custom programs written in LabVIEW (National Instruments, Austin, TX) with further data analysis in R to compute metrics of locomotory activity (STEGEMAN et al 2019).…”

“…In brief, we recorded video and quantified the swimming behavior of individual worms placed into 1.8µL droplets arranged in an array of 18 droplets on a glass slide as we manipulated temperature with custom hardware (STEGEMAN et al 2019). Image capture and processing of swimming worms was performed with custom programs written in LabVIEW (National Instruments, Austin, TX) with further data analysis in R to compute metrics of locomotory activity (STEGEMAN et al 2019). Our standard assay involved an increasing temperature regime from 25°C to 41°C with 1°C steps occurring every 80 s, recording video of the behavior for the last 20 s of each temperature step at 15fps.…”