Evolution and plasticity of thermal performance: an analysis of variation in thermal tolerance and fitness in 22 Drosophila species

Abstract

The thermal biology of ectotherms is often used to infer species' responses to changes in temperature. It is often proposed that temperate species are more cold-tolerant, less heat-tolerant, more plastic, have broader thermal performance curves (TPCs) and lower optimal temperatures when compared to tropical species. However, relatively little empirical work has provided support for this using large interspecific studies. In the present study, we measure thermal tolerance limits and thermal performance in 22 species of Drosophila that developed under common conditions. Specifically, we measure thermal tolerance (CT min and CT max ) as well as the fitness components viability, developmental speed and fecundity at seven temperatures to construct TPCs for each of these species. For 10 of the species, we also measure thermal tolerance and thermal performance following developmental acclimation to three additional temperatures. Using these data, we test several fundamental hypotheses about the evolution and plasticity of heat and cold resistance and thermal performance. We find that cold tolerance (CT min ) varied between the species according to the environmental temperature in the habitat from which they originated. These data support the idea that the evolution of cold tolerance has allowed species to persist in colder environments. However, contrary to expectation, we find that optimal temperature ( T opt ) and the breadth of thermal performance ( T breadth ) are similar in temperate, widespread and tropical species and we also find that the plasticity of TPCs was constrained. We suggest that the temperature range for optimal thermal performance is either fixed or under selection by the more similar temperatures that prevail during growing seasons. As a consequence, we find that T opt and T breadth are of limited value for predicting past, present and future distributions of species. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.

Impacts of thermal fluctuations on heat tolerance and its metabolomic basis across plant and animal species

“…This agrees with studies on plants that have found strong correlations between latitudinal temperature variability and plasticity of various fitness-related traits, including photosynthetic rate, water-use efficiency, seed-output, leaf angles and number of flowers [37,56,57]. Such association between latitudinal temperature variability and fitness-related traits and heat tolerance has generally been much weaker for insects [14,15,34,58]. Although we cannot make any conclusions on why plants in general respond stronger to thermal fluctuation based on our study, it could be speculated that plants have developed stronger plastic responses as a consequence of their sessile lifestyle compared to invertebrates.…”

“…temperature within days or seasons, plasticity will thus be important for survival when there is little time for evolutionary responses [27][28][29][30][31][32]. Many studies have examined if associations exists between environmental temperature variability of natural habitats and the degree of plasticity of thermal tolerance in animal ectotherms (reviewed by Addo-Bediako et al [21]; Hoffmann et al [30]; see also [33][34][35]), and plants [36][37][38][39]. In the studies with animals no relationship between the latitudinal origin of populations and the level of plasticity in thermotolerance is found, whereas the findings are conflicting for plant studies.…”

Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world

“…They found that tropical insects will be the most impacted by climate warming owing to their higher sensitivity to temperature changes and proximity of their living conditions to their optimal temperature. By contrast, a recent study on 22 Drosophila species reared under a common garden design (MacLean et al ., ) found that thermal performance curves are not as accurate as thermal limits for predicting climate‐driven range shifts. Still, particularly for insects, it remains to be determined whether thermal tolerance is a better predictor of climate‐driven range shifts than other life‐history traits (Table ; MacLean & Beissinger, ).…”

Quantitative genetics of temperature performance curves ofNeurospora crassa

“…While several studies have tested how different species or populations differ in their thermal performance curves, or if evolution has been able to shape them (e.g. Krenek et al ., 2011; Ketola and Saarinen, 2015; Ashrafi et al ., 2018; Maclean et al ., 2019), only a few studies have determined the evolutionary potential of thermal performance curves. In these studies, the genetic variance-covariance matrix (G-matrix) for thermal performance across several temperatures has been estimated, and how genetic variation is aligned with characteristic directions of reaction norm evolution has been determined (e.g.…”