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- Different Genomic Changes Underlie Adaptive Evolution in Populations of Contrasting HistoryPublication . Seabra, Sofia G; De mendonça fragata almeida, Inês; Antunes, Marta; Faria, Gonçalo S; Santos, MA; Sousa, Vitor C; Simões, Pedro; Matos, MargaridaExperimental evolution is a powerful tool to understand the adaptive potential of populations under environmental change. Here, we study the importance of the historical genetic background in the outcome of evolution at the genome-wide level. Using the natural clinal variation of Drosophila subobscura, we sampled populations from two contrasting latitudes (Adraga, Portugal and Groningen, Netherlands) and introduced them in a new common environment in the laboratory. We characterized the genome-wide temporal changes underlying the evolutionary dynamics of these populations, which had previously shown fast convergence at the phenotypic level, but not at chromosomal inversion frequencies. We found that initially differentiated populations did not converge either at genome-wide level or at candidate SNPs with signs of selection. In contrast, populations from Portugal showed convergence to the control population that derived from the same geographical origin and had been long-established in the laboratory. Candidate SNPs showed a variety of different allele frequency change patterns across generations, indicative of an underlying polygenic basis. We did not detect strong linkage around candidate SNPs, but rather a small but long-ranging effect. In conclusion, we found that history played a major role in genomic variation and evolution, with initially differentiated populations reaching the same adaptive outcome through different genetic routes.
- 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.
- 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.
- Long-term evolution experiments fully reveal the potential for thermal adaptationPublication . Antunes, Marta; Grandela, Afonso; Matos, Margarida; Simões, PedroEvolutionary responses may be crucial in allowing organisms to cope with prolonged effects of climate change. However, a clear understanding of the dynamics of adaptation to warming environments is still lacking. Addressing how reproductive success evolves in such deteriorating environments is extremely relevant, as this trait is constrained at temperatures below critical thermal limits. Experimental evolution under a warming environment can elucidate the potential of populations to respond to rapid environmental changes. The few studies following such framework lack analysis of long-term response. We here focus on the long-term thermal evolution of two Drosophila subobscura populations, from different European latitudes, under warming temperatures. We tested reproductive success of these populations in the ancestral (control) and warming environment after ∼50 generations of thermal evolution. We found a general adaptive response to warming temperatures in the long term, since populations evolving in the warming environment showed increased performance in that environment relative to the respective control populations. On the other hand, no clear response was observed in the ancestral environment. Coupled with data from previous generations, we highlight a slow pace of adaptive response and differences in that response between populations of distinct histories. These findings demonstrate the need of long-term evolution experiments to fully reveal the potential for thermal adaptation. It also highlights that the scrutiny of different populations is needed as a measure of variation in evolutionary responses within a species. Accounting for these sources of variation - both temporal and spatial - will allow for more robust assessments of climate change evolutionary responses.
- Detrimental impact of a heatwave on male reproductive behaviour and fertilityPublication . Grandela, Afonso; Antunes, Marta; Santos, Marta A.; Matos, Margarida; Rodrigues, Leonor R; Simões, PedroUnderstanding how heatwaves impact on different aspects of mating behaviour and fertility is getting increasingly important. In this context, laboratory fertility and mating experiments involving manipulation and exposure of insects to different thermal conditions are common procedures. To conduct such experiments practical methods such as dyes are needed for an easy, non-invasive discrimination of individuals. We report here a study measuring the effect of an extended heat stress applied to males on several parameters of mating behaviour and fertility of laboratory populations of Drosophila subobscura derived from two distinct European locations. We found highly detrimental effects of heatwave on mating behaviour—with longer (courtship and copulation) latencies and lower mating occurrence but no changes in mating duration—and fertility, with reduced fecundity and reproductive success. Furthermore, we also tested the efficacy of food dye as a marker for individual discrimination and mating occurrence. While food dye did not allow to infer the occurrence of a mating based on a transfer of coloration from male to female, it did not affect mating and fertility, attesting its utility has a method for discriminating individuals within mating experiments in the context of thermal studies. Importantly, despite the fact that the heatwave was only applied in males, we observed an impact on behaviour of females that mated with stressed males, by often refusing their nuptial feeding. This opens possibilities for further integrated research on the changes of female and male mating behaviour and fertility under different thermal scenarios.
- 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.
- Experimental Evolution in a Warming World: The Omics EraPublication . Santos, Marta A.; Carromeu-Santos, Ana; Quina, Ana S; Antunes, Marta; Kristensen, Torsten N; Santos, Mauro; Matos, Margarida; De mendonça fragata almeida, Inês; Simões, PedroA 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 (evolve and resequence) is a highly effective tool that has been increasingly employed to elucidate the genetic basis of adaptation. The number of thermal evolve and resequence 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 behavioral 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 standardization of methodologies and the utilization of new technologies focusing on the integration of genomic and phenotypic variation in the context of thermal adaptation.
- 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.
- 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.