Understanding how species respond to environmental changes is becoming increasingly important in order to predict the future of biodiversity and species distributions under current global warming conditions (Rezende 2020; Bennett et al 2021). Two key factors to take into account in these predictions are the tolerance of organisms to heat stress and subsequently how they adapt to increasingly warmer temperatures. Coupled with this, one important factor that is often overlooked when addressing the evolution of thermal tolerance, is the correlated responses in traits that are important to fitness, such as life histories, behavior and the underlying metabolic processes.

The rate and intensity of the thermal stress are expected to be major factors in shaping the evolution of heat tolerance and correlated responses in other traits. For instance, lower rates of thermal stress are predicted to select for individuals with a slower metabolism (Santos et al 2012), whereas low metabolism is expected to lead to a lower reproductive rate (Dammhahn et al 2018). To quantify the importance of the rate and intensity of thermal stress on the evolutionary response of heat tolerance and correlated response in behavior, Mesas et al (2021) performed experimental evolution in Drosophila subobscura using selective regimes with slow or fast ramping protocols. Whereas both regimes showed increased heat tolerance with similar evolutionary rates, the correlated responses in thermal performance curves for locomotor behavior differed between selection regimes. These findings suggest that thermal rate and intensity may shape the evolution of correlated responses in other traits, urging the need to understand possible correlated responses at relevant levels such as life history and metabolism. 

In the present contribution, Mesas and Castañeda (2022) investigate whether the disparity in thermal performance curves observed in the previous experiment (Mesas et al 2021) could be explained by differences in metabolic energy production and consumption, and how this correlated with the reproductive output (fecundity and viability). Overall, the authors show some evidence for lowered enzyme activity and increased performance in life-history traits, particularly for the slow-ramping selected flies. Specifically, the authors observe a reduction in glucose metabolism and increased viability when evolving under slow ramping stress. Interestingly, both regimes show a general increase in fecundity, suggesting that adaptation to these higher temperatures is not costly (for reproduction) in the ancestral environment. The evidence for a somewhat lower metabolism in the slow-ramping lines suggests the evolution of a slow “pace of life”. The “pace of life” concept tries to bridge variation across several levels namely metabolism, physiology, behavior and life history, with low “pace of life” organisms presenting lower metabolic rates, later reproduction and higher longevity than fast “pace of life” organisms (Dammhahn et al 2018, Tuzun & Stocks 2022).  As the authors state there is not a clear-cut association with the expectations of the pace of life hypothesis since there was evidence for increased reproductive output under both selection intensity regimes. This suggests that, given sufficient trait genetic variance, positively correlated responses may emerge during some stages of thermal evolution. As fecundity estimates in this study were focussed on early life, the possibility of a decrease in the cumulative reproductive output of the selected flies, even under benign conditions, cannot be excluded. This would help explain the apparent paradox of increased fecundity in selected lines. In this context, it would also be interesting to explore the variation in reproductive output at different temperatures, i.e to obtain thermal performance curves for life histories. 

Mesas and Castañeda (2022) raise important questions to pursue in the future and contribute to the growing evidence that, in order to predict the distribution of ectothermic species under current global warming conditions, we need to expand beyond determining the physiological thermal limits of each organism (Parratt et al 2021). Ultimately, integrating metabolic, life-history and behavioral changes during evolution under different thermal stresses within a coherent framework is key to developing better predictions of temperature effects on natural populations.  

References

Bennett, J.M., Sunday, J., Calosi, P. et al. The evolution of critical thermal limits of life on Earth. Nat Commun 12, 1198 (2021). https://doi.org/10.1038/s41467-021-21263-8

Dammhahn, M., Dingemanse, N.J., Niemelä, P.T. et al. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72, 62 (2018). https://doi.org/10.1007/s00265-018-2473-y

Mesas, A,  Jaramillo, A,  Castañeda, LE.  Experimental evolution on heat tolerance and thermal performance curves under contrasting thermal selection in Drosophila subobscura. J Evol Biol  34, 767– 778 (2021). https://doi.org/10.1111/jeb.13777

Mesas, A, Castañeda, LE Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura. bioRxiv, 2022.02.03.479001, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.03.479001

Parratt, S.R., Walsh, B.S., Metelmann, S. et al. Temperatures that sterilize males better match global species distributions than lethal temperatures. Nat. Clim. Chang. 11, 481–484 (2021). https://doi.org/10.1038/s41558-021-01047-0

Santos, M, Castañeda, LE, Rezende, EL Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits? Ecology and evolution, 2(11), 2866-2880 (2012). https://doi.org/10.1002/ece3.385

Tüzün, N, Stoks, R. A fast pace-of-life is traded off against a high thermal performance. Proceedings of the Royal Society B, 289(1972), 20212414 (2022). https://doi.org/10.1098/rspb.2021.2414

Rezende, EL, Bozinovic, F, Szilágyi, A, Santos, M. Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242-1245  (2020). https://doi.org/10.1126/science.aba9287