Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance

Abstract

Summary Thermal limits of ectotherms have been studied extensively and are believed to be evolutionarily constrained, leaving ectotherms at risk under future climate change. Phenotypic plasticity may extend the thermal limits, but we lack detailed characterizations of thermal limit reaction norms as well as an understanding of the interspecific variation in these reaction norms. Here, we investigated the interspecific variation in phenotypic plasticity of thermal limits in 13 Drosophila species. We obtained high‐resolution reaction norms for upper and lower thermal limits across the permissive developmental thermal range (12·5–30 °C). The estimated phenotypes were then associated (while accounting for phylogeny) with climatic parameters from the species’ distributional range. All species showed linear reaction norms for cold tolerance (CTmin) and heat tolerance (CTmax) across developmental acclimation temperatures. We observed strong beneficial cold acclimation to lower temperatures in all species. Conversely, the heat acclimation response was non‐existent in some species, and decreasing or increasing with increasing developmental acclimation temperatures in other species. The degree of phenotypic plasticity of CTmin and CTmax was related neither to the basal thermal limits (trade‐off hypothesis) nor to climatic parameters connected to latitudinal distributions (latitudinal hypothesis). A substantial and linear developmental plasticity of lower thermal limits is a general characteristic of Drosophila species, which allows for straightforward application in species distribution models. In general, upper thermal limits also show linear norms of reaction, but their adaptive significance is limited and highly variable among species, making general predictions across species rather impossible. High‐resolution estimates of norms of reaction of thermal limits can considerably increase our understanding of the capacity of ectotherms to acclimate to different thermal environments. However, our understanding of the environmental drivers of the evolution of phenotypic plasticity and thus of the interspecific differences remains ambiguous, potentially constrained by limited microclimate information. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12782/suppinfo is available for this article.

Biotic and abiotic factors investigated in two Drosophila species – evidence of both negative and positive effects of interactions on performance

“…In terms of the effect of developmental temperature on thermal tolerance, we also found different results in the two species. While a low developmental temperature resulted in a high cold tolerance and low heat tolerance in D. melanogaster , exposure of D. hydei to low developmental temperature resulted in significantly higher cold tolerance and unaltered heat tolerance compared to flies developed at an intermediate temperature, confirming results from other studies providing evidence for thermal acclimation29. The two species responded similarly in cold and heat tolerance to development at a high temperature, i.e.…”

“…Data was treated and cross-referenced using methods described in Schou et al . (in press)29. Thus the thermal regimes employed in this study are well within the range of what the two species will experience in their natural habitats.…”

Evidence for lower plasticity in CTMAX at warmer developmental temperatures

“…At the interspecific level, significant adult hardening responses in heat knockdown have been shown in a number of Drosophila species (Kellett et al ., ; Mitchell et al ., ); although plasticity was only weakly associated with the environment (southern latitude used as a proxy for environment) in one study (Mitchell et al ., ), such that tropical species tended to be less plastic than their widespread counterparts. Significant developmental acclimation effects have also been detected at the interspecific level in Drosophila for CT MAX , but plasticity was unrelated to the species’ environment or latitude of origin (Overgaard et al ., ; Schou et al ., ). These results suggest that Drosophila species, in general, have varying capacities to increase their upper thermal limits via plasticity and that this variation is unlikely to be predictably shaped by environmental selection (for further discussion, see Sorensen et al ., ).…”

Experimental Approaches for Testing if Tolerance Curves Are Useful for Predicting Fitness in Fluctuating Environments

“…Such curves are typically obtained by assessing the performance of genotypes in different constant environments; e.g., at a range of constant temperatures (e.g., Schou et al, 2016). Observations from these experiments allow researchers to get detailed information on performance across environmental gradients and they have been proposed to allow spatial and temporal visualization of fitness components of genotypes, and thereby for example pinpointing species or populations that are specialists or generalists, and for detecting genotype by environment interactions (Dobzhansky and Spassky, 1963).…”

“…Observations from these experiments allow researchers to get detailed information on performance across environmental gradients and they have been proposed to allow spatial and temporal visualization of fitness components of genotypes, and thereby for example pinpointing species or populations that are specialists or generalists, and for detecting genotype by environment interactions (Dobzhansky and Spassky, 1963). Tolerance curves have multiple purposes in diverse biological disciplines and they seem attractive for predicting performance and distribution of species in more natural fluctuating environments (Kassen, 2002;Chevin et al, 2010;Schou et al, 2016;Sexton et al, 2016).…”