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Generalitat de Catalunya. Funding sources had no involvement at any stage of the experiment or manuscript preparation.

Phenotypic plasticity can be an important tool in helping organisms to cope with changing thermal conditions and it may show an interdependency between life-stages. For instance, exposure to stressful temperatures during development can trigger a positive plastic response in adults. In this study, we analyse the thermal plastic response of laboratory populations of Drosophila subobscura, derived from two contrasting latitudes of the European cline. We measured fecundity characters in the experimental populations after exposure to five thermal treatments, with different combinations of developmental and adult temperatures (14°C, 18°C or 26°C). We ask whether (1) adult performance is enhanced (or reduced) by exposing flies to higher (or lower) temperatures during development only; (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 any evidence for historical effects on adult performance. Our main findings show that (1) higher developmental temperatures led to low reproductive performance regardless of adult temperature, while at lower temperatures reduced performance only occurred when cold conditions were persistent across juvenile and adult stage; (2) flies raised at lower temperatures did not always outperform those developed at other temperatures; (3) there was no (negative) cumulative effect of 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 a critical and most vulnerable stage to climate change and associated heat waves.

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Genes with relevant roles in the differentiation of closely-related species are likely to have diverged simultaneously with the species and more accurately reproduce the species tree. The Lusitanian (Microtus lusitanicus) and Mediterranean (M. duodecimcostatus) pine voles are two recently separated sister species with fossorial lifestyles whose different ecological, physiological and morphological phenotypes reflect the better adaptation of M. duodecimcostatus to the underground habitat. Here we asked whether the differentiation of M. lusitanicus and M. duodecimcostatus involved genetic variations within the tumour suppressor p53 gene, given its role in stress-associated responses. We performed a population-genetic analysis through sequencing of exons and introns of p53 in individuals from sympatric and allopatric populations of both the species in the Iberian Peninsula in which a unidirectional introgression of mitochondrial DNA was previously observed. We were able to discriminate the two species to a large extent. We show that M. duodecimcostatus is composed of one genetically unstructured group of populations sharing a P53 protein that carries a mutation in the DNA-binding region not observed in M. lusitanicus, raising the possibility that this mutation may have been central in the evolutionary history of M. duodecimcostatus. Our results provide suggestive evidence for the involvement of a master transcription factor in the separation of M. lusitanicus and M. duodecimcostatus during Microtus radiation in the Quaternary presumably via a differential adaptive role of the novel p53 in M. duodecimcostatus.

Adaptive evolution is key in mediating responses to climate change. Such evolution will expectedly lead to changes in the thermal reaction norms of populations and improve their ability to cope with stressful conditions. Conversely, constraints of different nature 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 changes of flies evolving for nine generations in a daily fluctuating environment with average constant temperature, or a warming environment with increasing average and amplitude temperature across generations. Our results showed that (1) evolution under a global warming scenario has not led, so far, to a noticeable change in the thermal response; (2) historical background appears to be affecting the responses of populations under the warming environment, particularly at higher temperatures; (3) thermal reaction norms are trait-dependent: while lifelong exposure to low temperature decreases fecundity and productivity but not viability, high temperature causes negative transgenerational effects on productivity and viability, even though fecundity remains high. These findings raise concerns about the short-term efficiency of adaptive responses to the current changing climate.

Adaptation 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.