Experimental evolution in a warming world - the omics era.

A comprehensive understanding of the genetic mechanisms that shape species responses to thermal variation is essential for more accurate predictions of the impacts of climate change on biodiversity. Experimental evolution with high-throughput resequencing approaches (E&R) is a highly effective tool that has been increasingly employed to elucidate the genetic basis of adaptation. The number of thermal E&R studies is rising, yet there is a dearth of efforts to integrate this new wealth of knowledge. Here we review this literature showing how these studies have contributed to increase our understanding on the genetic basis of thermal adaptation. We identify two major trends: highly polygenic basis of thermal adaptation and general lack of consistency in candidate targets of selection between studies. These findings indicate that the adaptive responses to specific environments are rather independent. A review of the literature reveals several gaps in the existing research. Firstly, there is a paucity of studies done with organisms of diverse taxa. Secondly, there is a need to apply more dynamic and ecologically relevant thermal environments. Thirdly, there is a lack of studies that integrate genomic changes with changes in life-history and behavioural traits. Addressing these issues would allow a more in-depth understanding of the relationship between genotype and phenotype. We highlight key methodological aspects that can address some of the limitations and omissions identified. These include the need for greater standardisation of methodologies and the utilisation of new technologies focusing on the integration of genomic and phenotypic variation in the context of thermal adaptation.

Heat-induced female biased sex ratio during development is not mitigated after prolonged thermal selection.

BACKGROUND: The negative impacts of climate change on biodiversity are consistently increasing. Developmental stages are particularly sensitive in many ectotherms. Moreover, sex-specific differences in how organisms cope with thermal stress can produce biased sex ratios upon emergence, with potentially major impacts on population persistence. This is an issue that needs investigation, particularly testing whether thermal selection can alleviate sex ratio distortions in the long-term is a critical but neglected issue. Here, we report an experiment analyzing the sex ratio patterns at different developmental temperatures in Drosophila subobscura populations subjected to long-term experimental evolution (~ 30 generations) under a warming environment. RESULTS: We show that exposure to high developmental temperatures consistently promotes sex ratio imbalance upon emergence, with a higher number of female than male offspring. Furthermore, we found that thermal selection resulting from evolution in a warming environment did not alleviate such sex ratio distortions generated by heat stress. CONCLUSIONS: We demonstrate that heat stress during development can lead to clear sex ratio deviations upon emergence likely because of differential survival between sexes. In face of these findings, it is likely that sex ratio deviations of this sort occur in natural populations when facing environmental perturbation. The inability of many insects to avoid thermal shifts during their (more) sessile developmental stages makes this finding particularly troublesome for population subsistence in face of climate warming events.

Past history shapes evolution of reproductive success in a global warming scenario.

Adaptive evolution is critical for animal populations to thrive in the fast-changing natural environments. Ectotherms are particularly vulnerable to global warming and, although their limited coping ability has been suggested, few real-time evolution experiments have directly accessed their evolutionary potential. Here, we report a long-term experimental evolution study addressing the evolution of Drosophila thermal reaction norms, after ∼30 generations under different dynamic thermal regimes: fluctuating (daily variation between 15 and 21 °C) or warming (daily fluctuation with increases in both thermal mean and variance across generations). We analyzed the evolutionary dynamics of Drosophila subobscura populations as a function of the thermally variable environments in which they evolved and their distinct background. Our results showed clear differences between the historically differentiated populations: high latitude D. subobscura populations responded to selection, improving their reproductive success at higher temperatures whereas their low latitude counterparts did not. This suggests population variation in the amount of genetic variation available for thermal adaptation, an aspect that needs to be considered to allow for better predictions of future climate change responses. Our results highlight the complex nature of thermal responses in face of environmental heterogeneity and emphasize the importance of considering inter-population variation in thermal evolution studies.

No evidence for short-term evolutionary response to a warming environment in Drosophila.

Adaptive evolution is key in mediating responses to global warming and may sometimes be the only solution for species to survive. Such evolution will expectedly lead to changes in the populations' thermal reaction norm and improve their ability to cope with stressful conditions. Conversely, evolutionary constraints might limit the adaptive response. Here, we test these expectations by performing a real-time evolution experiment in historically differentiated Drosophila subobscura populations. We address the phenotypic change after nine generations of evolution in a daily fluctuating environment with average constant temperature, or in a warming environment with increasing average and amplitude temperature across generations. Our results showed that (1) evolution under a global warming scenario does not lead to a noticeable change in the thermal response; (2) historical background appears to be affecting responses under the warming environment, particularly at higher temperatures; and (3) thermal reaction norms are trait dependent: although lifelong exposure to low temperature decreases fecundity and productivity but not viability, high temperature causes negative transgenerational effects on productivity and viability, even with high fecundity. These findings in such an emblematic organism for thermal adaptation studies raise concerns about the short-term efficiency of adaptive responses to the current rising temperatures.

High developmental temperature leads to low reproduction despite adult temperature.

Phenotypic plasticity can help organisms cope with changing thermal conditions and it may depend on which life-stage the thermal stress is imposed: for instance, exposure to stressful temperatures during development can trigger a positive plastic response in adults. Here, we analyze the thermal plastic response of laboratory populations of Drosophila subobscura, derived from two contrasting latitudes of the European cline. We measured reproductive performance through fecundity characters, after the experimental populations were exposed to five thermal treatments, with different combinations of developmental and adult temperatures (14 °C, 18 °C, or 26 °C). Our questions were whether (1) adult performance changes with exposure to higher (or lower) temperatures during development; (2) flies raised at lower temperatures outperform those developed at higher ones, supporting the "colder is better" hypothesis; (3) there is a cumulative effect on adult performance of exposing both juveniles and adults to higher (or lower) temperatures; (4) there is evidence for biogeographical effects on adult performance. Our main findings were that (1) higher developmental temperatures led to low reproductive performance regardless of adult temperature, while at lower temperatures reduced performance only occurred when colder conditions were persistent across juvenile and adult stages; (2) flies raised at lower temperatures did not always outperform those developed at other temperatures; (3) there were no harmful cumulative effects after exposing both juveniles and adults to higher temperatures; (4) both latitudinal populations showed similar thermal plasticity patterns. The negative effect of high developmental temperature on reproductive performance, regardless of adult temperature, highlights the developmental stage as very critical and most vulnerable to climate change and associated heat waves.

Beneficial developmental acclimation in reproductive performance under cold but not heat stress.

Thermal plasticity can help organisms coping with climate change. In this study, we analyse how laboratory populations of the ectotherm species Drosophila subobscura, originally from two distinct latitudes and evolving for several generations in a stable thermal environment (18 °C), respond plastically to new thermal challenges. We measured adult performance (fecundity traits as a fitness proxy) of the experimental populations when exposed to five thermal regimes, three with the same temperature during development and adulthood (15-15 °C, 18-18 °C, 25-25 °C), and two where flies developed at 18 °C and were exposed, during adulthood, to either 15 °C or 25 °C. Here, we test whether (1) flies undergo stress at the two more extreme temperatures; (2) development at a given temperature enhances adult performance at such temperature (i.e. acclimation), and (3) populations with different biogeographical history show plasticity differences. Our findings show (1) an optimal performance at 18 °C only if flies were subjected to the same temperature as juveniles and adults; (2) the occurrence of developmental acclimation at lower temperatures; (3) detrimental effects of higher developmental temperature on adult performance; and (4) a minor impact of historical background on thermal response. Our study indicates that thermal plasticity during development may have a limited role in helping adults cope with warmer - though not colder - temperatures, with a potential negative impact on population persistence under climate change. It also emphasizes the importance of analysing the impact of temperature on all stages of the life cycle to better characterize the thermal limits.