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Disparate patterns of thermal adaptation between life stages in temperate vs. tropical Drosophila melanogaster

Many terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioral thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. Average maximum temperature of the warmest month of the year predicted embryonic thermal tolerance in tropical but not temperate sites. We further report that embryos live closer to their upper thermal limits than adultso—i.e., thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting dominance of heat-tolerant alleles. Together our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages in order to better predict adaptive limits. Impact Summary Climate change may threaten the extinction of many ectothermic species, unless populations can evolutionarily adapt to rising temperatures. Natural selection should favor individuals with higher heat tolerances in hotter environments. But recent studies have found that individuals from hot and cold places often have similar heat tolerances. This pattern may indicate that the evolution of heat tolerance is constrained. If this were true, then it would have dire consequences for species persistence under novel thermal conditions. An alternative explanation for lack of variation in heat tolerance is that mobile organisms don’t need higher heat tolerances to survive in hotter places. The majority of studies have focused on heat tolerance of the adult life stage. Yet, adults in many species are mobile organisms that can avoid extreme heat by seeking shelter in cooler microhabitats (e.g., shaded locations). In contrast, immobile life stages (e.g., insect eggs) cannot behaviorally avoid extreme heat. Thus, mobile and immobile life stages may face different thermal selection pressures that lead to disparate patterns of thermal adaptation across life stages. Here, we compared heat tolerances of fruit fly adults and eggs (Drosophila melanogaster) from populations in temperate North America and tropical locations around the globe. Consistent with previous studies, we found no differences among populations in adult heat tolerance. However, eggs from tropical flies were consistently more heat tolerant than eggs from North American flies. Further, eggs had lower heat tolerance than adults. Consequently, fly eggs in the hotter tropics may experience heat death more frequently than adult flies later in life. This may explain why patterns of divergence in heat tolerance were decoupled across life stages. These patterns indicate that thermal adaptation may be life-stage-specific and suggest that future work should characterize thermal traits across life stages to better understand the evolution of thermal limits.