Genetic architecture of the thermal tolerance landscape of Drosophila melanogaster

Abstract

Increased environmental temperatures associated with global warming strongly impact the natural populations of ectothermic species. Therefore, it is crucial to understand the genetic foundations and evolutionary potential of heat tolerance. However, heat tolerance and its genetic components depend on the methodology, making it difficult to predict the adaptive responses to global warming. Here, we measured the knockdown time for 100 lines from the Drosophila Genetic Reference Panel (DGRP) at four different static temperatures, and we estimated their thermal death time (TDT) curves, which incorporate the magnitude and the time of exposure to thermal stress. Through quantitative genetic analyses, it was observed that the knockdown time showed a significant heritability at different temperatures and that its genetic correlations decreased as temperatures were dissimilar. Significant genotype-by-sex and genotype-by-environment interactions were noted for knockdown time. We also discovered heritable variation for the two parameters of TDT: CTmax and thermal sensitivity. Taking advantage of the DGRP, we performed a GWAS and identified multiple variants positively associated with the TDT parameters, which map to genes related to signaling and developmental functions. We performed functional validations for some candidate genes using RNAi, which revealed that genes such as mam, KNCQ, or robo3 affect the knockdown time at a specific temperature but are not associated with the TDT parameters. Ultimately, the thermal tolerance landscape must possess the ability to adapt to the selective pressures caused by global warming. Genetic variation of phenotypic plasticity and sexually antagonistic pleiotropy should also facilitate the adaptive process and maintain the genetic diversity in Drosophila populations.