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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.
- Systematic approaches to assessing high-temperature limits to fertility in animalsPublication . Bretman, Amanda; Fricke, Claudia; Baur, Julian; Berger, David; Breedveld, Merel C; Dierick, Diego; Canal Domenech, Berta; Drobniak, Szymon M; Ellers, Jacintha; English, Sinead; Gasparini, Clelia; Iossa, Graziella; Lagisz, Malgorzata; Nakagawa, Shinichi; Noble, Daniel W A; Pottier, Patrice; Ramm, Steven A; Rowe, Melissah; Schultner, Eva; Schou, Mads; Simões, Pedro; Stockley, Paula; Vasudeva, Ramakrishnan; Weaving, Hester; Price, Tom A R; Snook, Rhonda RCritical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a “gold-standard” protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.
- 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.
- 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.
- 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.
- 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
- A systematic map of studies testing the relationship between temperature and animal reproductionPublication . Dougherty, Liam R.; Frost, Fay; Maenpaa, Maarit I.; Rowe, Melissah; Cole, Benjamin J.; Vasudeva, Ramakrishnan; Pottier, Patrice; Schultner, Eva; Macartney, Erin L.; Lindenbaum, Ina; Smith, Jamie L.; Carazo, Pau; Graziano, Marco; Weaving, Hester; Canal Domenech, Berta; Berger, David; Meena, Abhishek; Bishop, Tom Rhys; Noble, Daniel W. A.; Simões, Pedro; Baur, Julian; Breedveld, Merel C.; Svensson, Erik I.; Lancaster, Lesley T.; Ellers, Jacintha; De Nardo, Alessio N.; Santos, Marta A.; Ramm, Steven A.; Drobniak, Szymon M.; Redana, Matteo; Tuni, Cristina; Pilakouta, Natalie; Zizzari, Z. Valentina; Iossa, Graziella; Lüpold, Stefan; Koppik, Mareike; Early, Regan; Gasparini, Clelia; Nakagawa, Shinichi; Lagisz, Malgorzata; Bretman, Amanda; Fricke, Claudia; Snook, Rhonda R.; Price, Tom A. R.Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.
- 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.