Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance inDrosophila subobscura

Abstract

Adaptation to warming conditions involves increased heat tolerance and metabolic changes to reduce maintenance costs and maximize biological functions close to fitness. Evidence shows that energy metabolism evolves in response to warming conditions, but we know little about how heat stress intensity determines the evolutionary responses of metabolism and life history traits. Here, we evaluated the evolutionary responses of energy metabolism and life-history traits to artificial selection for increasing heat tolerance in Drosophila subobscura, using 2 protocols to measure and select heat tolerance: slow and fast ramping protocols. We found that the increase in heat tolerance was associated with reduced activity of the enzymes involved in the glucose-6-phosphate branchpoint but no changes of the metabolic rate in selected lines. We also found that the evolution of increased heat tolerance increased the early fecundity in selected lines and increased the egg-to-adult viability only in the slow-ramping selected lines. This work shows heat tolerance can evolve under different thermal scenarios but with different evolutionary outcomes on associated traits depending on the heat stress intensity. Therefore, spatial and temporal variability of thermal stress intensity should be taken into account to understand and predict the adaptive response to ongoing and future climatic conditions.

Cross-tolerance evolution is driven by selection on heat tolerance inDrosophila subobscura

“…As heritability is commonly used as a predictor of the evolutionary response of a trait to natural or artificial selection, it is expected that the evolutionary response of heat tolerance depends on the ramping rate used during selection. However, previous work did not support this prediction for D. subobscura , finding that the evolution of the knockdown temperature was independent of the ramping rate [26], but the correlated responses of the thermal performance curves or the energy metabolism depended on the intensity of the thermal selection [26,27]. Here, the evolution of knockdown temperature induced a correlated response on heat knockdown time when it was assayed at intermediate temperatures (36 and 37 °C), but not at less or more extreme assayed temperatures (35 and 38°C).…”

“…However, here the energy content was not measured in the different control and selected lines, which could have provided additional information about the evolutionary response in metabolite storage. However, body mass and metabolic rate were similar between control and selected lines [27], suggesting that neither difference in resource storage nor energy conservation explain sex-dependent correlated response for stress resistance traits. However, direct evaluation of the underlying mechanisms related to desiccation and starvation resistance should be explored to provide a better idea of the physiological basis of the evolution of stress resistance traits.…”

“…After three generations, each replicate cage was divided into four population cages. Thus, our experimental design had four different artificial selection protocols in triplicate: fast-ramping selection, fast-ramping control, slow-ramping selection, and slow-ramping control lines (see Mesas & Castañeda [27]). During the selection experiments, population cages were maintained at 18 °C (12:12 light-dark cycle) in a discrete generation, controlled larval density regime [40].…”

“…In particular, the experimental evolution of heat tolerance has been explored in multiple species, including fishes, corals, and insects [19][20][21][22]. Experimental evolution of heat tolerance has also been studied in several Drosophila species, including D. melanogaster [23,24] and D. subobscura [25][26][27], and D. buzzatti [28,29].…”

“…In particular, the experimental evolution of heat tolerance has been explored in multiple species, including fishes, corals, and insects [19–22]. Experimental evolution of heat tolerance has also been studied in several Drosophila species, including D. melanogaster [23,24] and D. subobscura [25–27], and D. buzzatti [28,29]. Most of these studies reported the evolution of heat tolerance using fast ramping protocols, ranging from 0.4 °C/min in Folk et al [24] to 1 °C/min in Gilchrist and Huey [23], or high-temperature static assays (40 °C), as in Bubliy and Loeschcke (28).…”