Pronounced plastic and evolutionary responses to unpredictable thermal fluctuations in <i>Drosophila simulans</i>

Organisms are exposed to temperatures that vary, for example on diurnal and seasonal time scales. Thus, the ability to behaviorally and/or physiologically respond to variation in temperatures is a fundamental requirement for long-term persistence. Studies on thermal biology in ectotherms are typically performed under constant laboratory conditions, which differ markedly from the variation in temperature across time and space in nature. Here, we investigate evolutionary adaptation and environmentally induced plastic responses of Drosophila simulans to no fluctuations (constant), predictable fluctuations or unpredictable fluctuations in temperature. We whole-genome sequenced populations exposed to 20 generations of experimental evolution under the three thermal regimes and examined the proteome after short-term exposure to the same three regimes. We find that unpredictable fluctuations cause the strongest response at both genome and proteome levels. The loci showing evolutionary responses were generally unique to each thermal regime, but a minor overlap suggests either common laboratory adaptation or that some loci were involved in the adaptation to multiple thermal regimes. The evolutionary response, i.e., loci under selection, did not coincide with induced responses of the proteome. Thus, genes under selection in fluctuating thermal environments are distinct from genes important for the adaptive plastic response observed within a generation. This information is key to obtain a better understanding and prediction of the effects of future increases in both mean and variability of temperatures

Mouse Genome-Wide Association Mapping Needs Linkage Analysis to Avoid False-Positive Loci

We carried out genome-wide association (GWA) studies in inbred mouse strains characterized for their lung tumor susceptibility phenotypes (spontaneous or urethane-induced) with panels of 12,959 (13K) or 138,793 (140K) single-nucleotide polymorphisms (SNPs). Above the statistical thresholds, we detected only SNP rs3681853 on Chromosome 5, two SNPs in the pulmonary adenoma susceptibility 1 (Pas1) locus, and SNP rs4174648 on Chromosome 16 for spontaneous tumor incidence, urethane-induced tumor incidence, and urethane-induced tumor multiplicity, respectively, with the 13K SNP panel, but only the Pas1 locus with the 140K SNP panel. Haplotype analysis carried out in the latter panel detected four additional loci. Loci reported in previous GWA studies failed to replicate. Genome-wide genetic linkage analysis in urethane-treated (BALB/c×C3H/He)F2, (BALB/c×SWR/J)F2, and (A/J×C3H/He)F2 mice showed that Pas1, but none of the other loci detected previously or herein by GWA, had a significant effect. The Lasc1 gene, identified by GWA as a functional element (Nat. Genet., 38:888–95, 2006), showed no genetic effects in the two independent intercross mouse populations containing both alleles, nor was it expressed in mouse normal lung or lung tumors. Our results indicate that GWA studies in mouse inbred strains can suffer a high rate of false-positive results and that such an approach should be used in conjunction with classical linkage mapping in genetic crosses

Data from: Environmental heterogeneity does not affect levels of phenotypic plasticity in natural populations of three Drosophila species

Adaptation of natural populations to variable environmental conditions may occur by changes in trait means and/or in the levels of plasticity. Theory predicts that environmental heterogeneity favors plasticity of adaptive traits. Here we investigated the performance in several traits of three sympatric Drosophila species freshly collected in two environments that differ in the heterogeneity of environmental conditions. Differences in trait means within species were found in several traits, indicating that populations differed in their evolutionary response to the environmental conditions of their origin. Different species showed distinct adaptation with a very different role of plasticity across species for coping with environmental changes. However, geographically distinct populations of the same species generally displayed the same levels of plasticity as induced by fluctuating thermal regimes. This indicates a weak and trait-specific effect of environmental heterogeneity on plasticity. Furthermore, similar levels of plasticity were found in a laboratory-adapted population of Drosophila melanogaster with a common geographic origin but adapted to the laboratory conditions for more than 100 generations. Thus, this study does not confirm theoretical predictions on the degree of adaptive plasticity among populations in relation to environmental heterogeneity but shows a very distinct role of species-specific plasticity

water content (Fig 3A)

Water content in flies exposed to ramping assay under different conditions (vial types

Data from: Few genetic and environmental correlations between life history and stress resistance traits affect adaptation to fluctuating thermal regimes

Laboratory selection in thermal regimes that differed in the amplitude and the predictability of daily fluctuations had a marked effect on stress resistance and life history traits in Drosophila simulans. The observed evolutionary changes are expected to be the result of both direct and correlated responses to selection. Thus, a given trait might not evolve independently from other traits because of genetic correlations among these traits. Moreover, different test environments can induce novel genetic correlations because of the activation of environmentally dependent genes. To test whether and how genetic correlations among stress resistance and life history traits constrain evolutionary adaptation, we used three populations of D. simulans selected for 20 generations in constant, predictable and unpredictable daily fluctuating thermal regimes and tested each of these selected populations in the same three thermal regimes. We explored the relationship between genetic correlations between traits and the evolutionary potential of D. simulans by comparing genetic correlation matrices in flies selected and tested in different thermal test regimes. We observed genetic correlations mainly between productivity, body size, starvation and desiccation tolerance, suggesting that adaptation to the three thermal regimes was affected by correlations between these traits. We also found that the correlations between some traits such as body size and productivity or starvation tolerance and productivity were determined by test regime rather than selection regime that is expected to limit genetic adaptation to thermal regimes in these traits. The results of this study suggest that several traits and several environments are needed to explore adaptive responses, as genetic and environmentally induced correlations between traits as results obtained in one environment cannot be used to predict the response of the same population in another environment

CTmax and oxygen

Heat tolerance (CTmax) as a function of oxygen limitatio

Read me

Overview of associated data file

water content (Fig 3B)

Water content in flies exposed to desiccation for different amounts of tim

Data from: Predictability rather than amplitude of temperature fluctuations determines stress resistance in a natural population of Drosophila simulans

The adaptability of organisms to novel environmental conditions depends on the amount of genetic variance present in the population as well as on the ability of individuals to adjust their phenotype through phenotypic plasticity. Here, we investigated the phenotypic plasticity induced by a single generation's exposure to three different temperature regimes with respect to several life-history and stress-resistance traits in a natural population of Drosophila simulans. We studied a constant as well as a predictably and an unpredictably fluctuating temperature regime. We found high levels of phenotypic plasticity among all temperature regimes, suggesting a strong influence of both temperature fluctuations and their predictability. Increased heat tolerance was observed for flies developed in both types of fluctuating thermal environments compared with flies developed in a constant environment. We suggest that this was due to beneficial hardening when developing in either fluctuating temperature environment. To our surprise, flies that developed in constant and predictably changing environments were similar to each other in most traits when compared to flies from the unpredictably fluctuating environment. The unpredictably changing thermal environment imposed the most stressful condition, resulting in the lowest performance for stress-related traits, even though the absolute temperature changes never exceeded that of the predictably fluctuating environment. The overall decreased stress resistance of flies in the unpredictably fluctuating environment may be the consequence of maladaptive phenotypic plasticity in this setting, indicating that the adaptive value of plasticity depends on the predictability of the environment

alltraitcor

Phenotypic data of several life history and stress resistance traits in 3 drosophila species from two environmentally markedly different location