Genetic Architecture of the Thermal Tolerance Landscape in Drosophila melanogaster

Increased environmental temperatures associated with global warming strongly impact natural populations of ectothermic species. Therefore, it is crucial to understand the genetic basis 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, to determine the genetic basis of the thermal tolerance landscape. Through quantitative genetic analyses, the knockdown time showed a significant heritability at different temperatures and that its genetic correlations decreased as temperatures differences increased. Significant genotype-by-sex and genotype-by-environment interactions were noted for heat tolerance. We also discovered genetic variability for the two parameters of TDT: CT_max and thermal sensitivity. Taking advantage of the DGRP, we performed a GWAS and identified multiple variants associated with the TDT parameters, which mapped to genes related to signalling 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. In conlusion, the thermal tolerance landscape display genetic variation and plastic responses, which may facilitate the adaptation of Drosophila populations to a changing world.