Temperature adaptation and its impact on the shape of performance curves inDrosophilapopulations

Abstract

Understanding how species adapt to different temperatures is crucial to predict their response to global warming, and thermal performance curves (TPCs) have been employed recurrently to study this topic. Nevertheless, fundamental questions regarding how thermodynamic constraints and evolution interact to shape TPCs in lineages inhabiting different environments remain unanswered. Here, we study Drosophila simulans along a latitudinal gradient spanning 3000 km to test opposing hypotheses based on thermodynamic constrains ( hotter-is-better ) versus biochemical adaptation ( jack-of-all-temperatures ) as primary determinants of TPCs variation across populations. We compare thermal responses in metabolic rate and the egg-to-adult survival as descriptors of organismal performance and fitness, respectively, and show that different descriptors of TPCs vary in tandem with mean environmental temperatures, providing strong support to hotter-is-better . Thermodynamic constraints also resulted in a strong negative association between maximum performance and thermal breadth. Lastly, we show that descriptors of TPCs for metabolism and egg-to-adult survival are highly correlated, providing evidence of co-adaptation, and that curves for egg-to-adult survival are systematically narrower and displaced toward lower temperatures. Taken together, our results support the pervasive role of thermodynamics constraining thermal responses in Drosophila populations along a latitudinal gradient, that are only partly compensated by evolutionary adaptation.

Phenotypic adaptation to temperature in the mosquito vector, Aedes aegypti

“…The modest extent of the shift could be because adaption is still ongoing after 10 generations, because differences in stable mean temperatures around the optimum impose limited selection pressure on overall thermal performance, or because there are limits to adaptive potential within our founding population. The slightly reduced operative range for the lines passaged at 31°C compared with those passaged at 27°C, together with a small reduction in maximum fitness, follows previous observations that warm-adapted lineages tend to exhibit narrower thermal performance curves than their colder adapted counterparts (Alruiz et al, 2023;Deutsch et al, 2008;Gaitán-Espitia et al, 2013) and are indicative of thermodynamic constraints on the extent of adaptive potential (Verhulst et al, 2020). Ultimately, there will be some limits to adaptation and there are examples of both alpine and tropical species of Drosophila that are predicted to be unable to adapt to warming temperatures, leading to expectations of range loss (Hoffmann et al, 2003;Kellermann et al, 2009;Kinzner et al, 2019).…”

Fitness surfaces and local thermal adaptation in Drosophila along a latitudinal gradient

“…In the specific case of our study, results show that Darwinian fitness decreases at higher latitudes (Figure 3). This is not in itself surprising, and the reconstructed surface not only supports the ‘hotter‐is‐better’ thermodynamic constraint hypothesis, which posits that evolutionary adaptation cannot entirely offset thermodynamic limitations (Alruiz et al., 2023; Huey & Kingsolver, 1989), but also illustrates how this constraint might translate into field conditions and quantifies by how much fitness is expected to decrease. Our approach can be combined with quantitative genetic analyses (Roff, 2002; Walsh & Lynch, 2018) to study rates of genetic and phenotypic adaptation to climate change.…”

“…Thus, performance curves from populations from colder regions become both wider and lower, indicating a trade‐off between thermal breadth and maximum performance, as discussed in detail in Alruiz et al. (2023).…”

“…As a result, maximum egg-to-adult viability decreased from 1.90 to 1.10 new adults day −1 with latitude, whereas thermal breadth where egg-to-adult viability surpasses 50% of the maximum increased from 9.0°C to 14.7°C (Figure S1). Thus, performance curves from populations from colder regions become both wider and lower, indicating a trade-off between thermal breadth and maximum performance, as discussed in detail in Alruiz et al (2023).…”

“…With this purpose, we constructed fitness surfaces based on environmental temperature data and simulated transplant experiments in silico. Empirical estimates of viability and heat tolerance for D. simulans as a function of temperature were published elsewhere in detail (Alruiz et al, 2022(Alruiz et al, , 2023, hence here we focus on how they can be combined to provide more realistic estimates of fitness and employed to study local adaptation from an analytical perspective. We assessed two criteria posited as evidence of local adaptation sensu strictu in transplant experiments (Blanquart et al, 2013;Kawecki & Ebert, 2004): (i) that local populations demonstrate superior fitness in their native environment compared to foreign populations ('local vs. foreign' criterion), and (ii) that fitness in one's own locality surpasses fitness in other locations ('home vs. away' criterion).…”