Abstract
Thermal tolerance of an organism depends on both the ability to dynamically adjust to a thermal stress and preparatory developmental processes that enhance thermal resistance. However, the extent to which standing genetic variation in thermal tolerance alleles influence dynamic stress responses vs. preparatory processes is unknown. Here, using the model species Drosophila melanogaster, we used a combination of Genome Wide Association mapping (GWAS) and transcriptomic profiling to characterize whether genes associated with thermal tolerance are primarily involved in dynamic stress responses or preparatory processes that influence physiological condition at the time of thermal stress. To test our hypotheses, we measured the critical thermal minimum (CTmin) and critical thermal maximum (CTmax) of 100 lines of the Drosophila Genetic Reference Panel (DGRP) and used GWAS to identify loci that explain variation in thermal limits. We observed greater variation in lower thermal limits, with CTmin ranging from 1.81 to 8.60°C, while CTmax ranged from 38.74 to 40.64°C. We identified 151 and 99 distinct genes associated with CTmin and CTmax, respectively, and there was strong support that these genes are involved in both dynamic responses to thermal stress and preparatory processes that increase thermal resistance. Many of the genes identified by GWAS were involved in the direct transcriptional response to thermal stress (72/151 for cold; 59/99 for heat), and overall GWAS candidates were more likely to be differentially expressed than other genes. Further, several GWAS candidates were regulatory genes that may participate in the regulation of stress responses, and gene ontologies related to development and morphogenesis were enriched, suggesting many of these genes influence thermal tolerance through effects on development and physiological status. Overall, our results suggest that thermal tolerance alleles can influence both dynamic plastic responses to thermal stress and preparatory processes that improve thermal resistance. These results also have utility for directly comparing GWAS and transcriptomic approaches for identifying candidate genes associated with thermal tolerance.
Highlights
Temperature directly affects performance, survival, fitness, and the geographic distribution of organisms (Angilletta, 2009; Dowd et al, 2015)
We tested for trade-offs associated with thermal tolerance by comparing critical thermal minimum (CTmin) and critical thermal maximum (CTmax) with previously collected lifespan and fecundity data (Durham et al, 2014); we found no evidence of trade-offs among these traits, as neither thermal tolerance measurement was correlated with longevity or fecundity (Supplementary Table 2)
Several studies have separately assessed the genetic architecture and plastic transcriptional responses to thermal stress, but the extent to which genes associated with thermal tolerance are involved in preparative and dynamic stress responses has not been assessed
Summary
Temperature directly affects performance, survival, fitness, and the geographic distribution of organisms (Angilletta, 2009; Dowd et al, 2015). Genetic variation in thermal tolerance is well-documented (e.g., Sørensen et al, 2001; McMillan et al, 2005; Rako et al, 2007) and can occur through changes in basal stress tolerance and/or changes in the ability to quickly respond to thermal challenges (Ayrinhac et al, 2004). These heritable differences within populations permit evolutionary shifts in thermal response as selection acts (Hoffmann et al, 2003), and adaptive differences in thermal tolerance across latitudinal gradients and thermal environments are common (Hoffmann et al, 2002; Fallis et al, 2014). Thermal tolerance is a trait that is both highly plastic and highly adaptable, and understanding the genetic basis of thermal tolerance is critical for predicting future responses to environmental change
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