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- Evolution and Plasticity of Gene Expression Under Progressive Warming in Drosophila subobscuraPublication . Antunes, Marta; Santos, Marta A.; Quina, Ana S.; Santos, Mauro; Matos, Margarida; Simões, PedroUnderstanding the molecular mechanisms of thermal adaptation is crucial to predict the impacts of global warming. However, there is still a lack of research on the effects of rising temperatures over time and of studies involving different populations from the same species. The present study focuses on these two aspects, which are of great importance in understanding how organisms cope and adapt to ongoing changes in their environment. This study investigates the impact of global warming on the gene expression patterns of Drosophila subobscura populations from two different latitudinal locations after 23 generations of evolution. Our results indicate that evolutionary changes depend on the genetic background of the populations, with different starting points for thermal evolution, and that high-latitude populations show more pronounced evolutionary changes, with some evidence of convergence towards low-latitude populations. We found an interplay between plasticity and selection, with the high-latitude population showing fewer initial plastic genes and lower levels of adaptive plasticity, but a greater magnitude of change in both plastic and selective responses during evolution under warming conditions compared with its low-latitude counterpart. A substantial proportion of the transcriptome was observed to be evolving, despite the lack of observable response at higher-order phenotypic traits. The interplay between plasticity and selection may prove to be an essential component in shaping species’ evolutionary responses to climate change. Furthermore, the value of conducting studies on multiple populations of the same species is emphasised, given the identification of differences between populations with different backgrounds in several contexts.
- Sex and population differences underlie variation in reproductive success in a warming environmentPublication . Santos, MA; Grandela, Afonso; Antunes, Marta; Quina, Ana S; Santos, Mauro; Matos, Margarida; Simões, PedroCurrent rising temperatures are threatening biodiversity. It is therefore crucial to understand how climate change impacts on male and female fertility and whether evolutionary responses can help in coping with heat stress. We use experimental evolution to study male and female fertility during real-time evolution of two historically differentiated populations of Drosophila subobscura under different thermal selection regimes for 23 generations. We aim to (1) tease apart sex-specific differences in fertility after exposure to warming conditions during development, (2) test whether thermal selection can enhance fertility under thermal stress, and (3) address the role of historically distinct genetic backgrounds. Contrary to expectations, heat stress during development had a higher negative impact on female fertility than on male fertility. We did not find clear evidence for enhanced fertility in male or females evolving under warming conditions. Population history had a clear impact on fertility response under thermal stress, particularly in males with those from lower latitude presenting better performance than their higher latitude counterparts. We show that the impact of thermal stress on fertility varies between traits, sexes and genetic backgrounds. Incorporating these several levels of variation is crucial for a deeper understanding of how fertility evolves under climate change.
- No evidence for short‐term evolutionary response to a warming environment in DrosophilaPublication . Santos, Marta A.; Carromeu‐Santos, Ana; Quina, Ana; Santos, Mauro; Matos, Margarida; Simões, PedroAdaptive 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 effciency of adaptive responses to the current rising temperatures.
- Slow and population specific evolutionary response to a warming environmentPublication . Santos, Marta A.; Antunes, Marta; Grandela, Afonso; Quina, Ana S.; Santos, Mauro; Matos, Margarida; Simões, PedroAdaptation to increasingly warmer environments may be critical to avoid extinction. Whether and how these adaptive responses can arise is under debate. Though several studies have tackled evolutionary responses under different thermal selective regimes, very few have specifically addressed the underlying patterns of thermal adaptation under scenarios of progressive warming conditions. Also, considering how much past history affects such evolutionary response is critical. Here, we report a long-term experimental evolution study addressing the adaptive response of Drosophila subobscura populations with distinct biogeographical history to two thermal regimes. Our results showed clear differences between the historically differentiated populations, with adaptation to the warming conditions only evident in the low latitude populations. Furthermore, this adaptation was only detected after more than 30 generations of thermal evolution. Our findings show some evolutionary potential of Drosophila populations to respond to a warming environment, but the response was slow and population specific, emphasizing limitations to the ability of ectotherms to adapt to rapid thermal shifts.
- Heat-induced female biased sex ratio during development is not mitigated after prolonged thermal selectionPublication . Santos, Marta A.; Antunes, Marta; Grandela, Afonso; Carromeu-Santos, Ana; Quina, Ana; Santos, Mauro; Matos, Margarida; Simões, PedroBackground The negative impacts of climate change on biodiversity are consistently increasing. Developmen‑ tal stages are particularly sensitive in many ectotherms. Moreover, sex-specifc diferences 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 diferent 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 ofspring. Furthermore, we found that thermal selec‑ tion 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 diferential survival between sexes. In face of these fndings, 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.
- Playing evolution in the laboratory: From the first major evolutionary transition to global warmingPublication . De mendonça fragata almeida, Inês; Simões, Pedro; Matos, Margarida; Szathmáry, Eörs; Santos, MauroExperimental evolution allows testing hypothesis derived from theory or from observed patterns in nature. We have designed a droplet-based microfluidic ‘evolution machine’ to test how transient compartmentalization (‘trait-groups’) of independent molecular replicators (likely a critical step in the origin of life) could have prevented the spread of parasitic mutants; that is, inactive RNAs that have been reported to spoil a system of free replicators. In remarkable agreement with the theory, we show that this simple population structure was sufficient to prevent takeover by inactive RNAs. A more complex scenario arises when we use experimental evolution to test field-derived hypothesis; for instance, the idea that temperature is driving genetic spatiotemporal patterns of climate change. In the fly Drosophila subobscura, latitudinal clines in gene arrangement frequencies occur worldwide, and more equatorial gene arrangements are becoming more frequent at higher latitudes as a correlated response to climate change. However, the evolution at different constant temperatures in the laboratory was not consistent with patterns in nature, suggesting some limitations of experimental evolution. Finally, also in D. subobscura, we show that repeatability in experimental evolution is staggeringly consistent for life history traits, making evolution quite predictable and suggesting that laboratory selection can quickly erase differences between populations. Yet, the genetic paths used to attain the same adaptive phenotypes are complex and unpredictable.
- How phenotypic convergence arises in experimental evolutionPublication . Simões, Pedro; De mendonça fragata almeida, Inês; Santos, Josiane; Santos, Marta A.; Santos, Mauro; Rose, Michael R.; Matos, MargaridaEvolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a "real-time" or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short-term (∼20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short- and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long-established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.
- Predictable phenotypic, but not karyotypic, evolution of populations with contrasting initial historyPublication . Simões, Pedro; De mendonça fragata almeida, Inês; Seabra, Sofia G.; Faria, Gonçalo S.; Santos, Marta A.; Rose, Michael R.; Santos, Mauro; Matos, MargaridaThe relative impact of selection, chance and history will determine the predictability of evolution. There is a lack of empirical research on this subject, particularly in sexual organisms. Here we use experimental evolution to test the predictability of evolution. We analyse the real-time evolution of Drosophila subobscura populations derived from contrasting European latitudes placed in a novel laboratory environment. Each natural population was sampled twice within a three-year interval. We study evolutionary responses at both phenotypic (life-history, morphological and physiological traits) and karyotypic levels for around 30 generations of laboratory culture. Our results show (1) repeatable historical effects between years in the initial state, at both phenotypic and karyotypic levels; (2) predictable phenotypic evolution with general convergence except for body size; and (3) unpredictable karyotypic evolution. We conclude that the predictability of evolution is contingent on the trait and level of organization, highlighting the importance of studying multiple biological levels with respect to evolutionary patterns.
- Editorial: Coping With Climate Change: A Genomic Perspective on Thermal AdaptationPublication . Matos, Margarida; Simões, Pedro; De mendonça fragata almeida, Inês; Quina, Ana Sofia; Kristensen, Torsten Nigaard; Santos, Mauro
- Past history shapes evolution of reproductive success in a global warming scenarioPublication . Santos, Marta A.; Antunes, Marta; Grandela, Afonso; Carromeu-Santos, Ana; Quina, Ana S.; Santos, Mauro; Matos, Margarida; Simões, PedroAdaptive 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.