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Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes.

ABSTRACT: Little is known of how gene expression and its plasticity evolves as populations adapt to different environmental regimes. Expression is expected to evolve adaptively in all populations but only those populations experiencing environmental heterogeneity are expected to show adaptive evolution of plasticity. We measured the transcriptome in a cadmium-enriched diet and a salt-enriched diet for experimental populations of Drosophila melanogaster that evolved for ~130 generations in one of four selective regimes: two constant regimes maintained in either cadmium or salt diets and two heterogeneous regimes that varied either temporally or spatially between the two diets. For populations evolving in constant regimes, we find a strong signature of counter-gradient evolution; the evolved expression differences between populations adapted to alternative diets is opposite to the plastic response of the ancestral population that is naïve to both diets. Based on expression patterns in the ancestral populations, we identify a set of genes for which we predict selection in heterogeneous regimes to result in increases in plasticity and we find the expected pattern. In contrast, a set of genes where we predicted reduced plasticity did not follow expectation. Nonetheless, both gene sets showed a pattern consistent with adaptive expression evolution in heterogeneous regimes, highlighting the difference between observing "optimal" plasticity and improvements in environment-specific expression. Looking across all genes, there is evidence in all regimes of differences in biased allele expression across environments ("allelic plasticity") and this is more common among genes with plasticity in total expression.

SUBMITTER: Huang Y

PROVIDER: S-EPMC5035091 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes.

Huang Yuheng Y Agrawal Aneil F AF

PLoS genetics 20160923 9

Little is known of how gene expression and its plasticity evolves as populations adapt to different environmental regimes. Expression is expected to evolve adaptively in all populations but only those populations experiencing environmental heterogeneity are expected to show adaptive evolution of plasticity. We measured the transcriptome in a cadmium-enriched diet and a salt-enriched diet for experimental populations of Drosophila melanogaster that evolved for ~130 generations in one of four sele ...[more]

PMID: 27661078

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Project description:BackgroundIndividual organisms may exhibit phenotypic plasticity when they acclimate to different conditions. Such plastic responses may facilitate or constrain the adaptation of their descendant populations to new environments, complicating their evolutionary trajectories beyond the genetic blueprint. Intriguingly, phenotypic plasticity itself can evolve in terms of its direction and magnitude during adaptation. However, we know little about what determines the evolution of phenotypic plasticity, including gene expression plasticity. Recent laboratory-based studies suggest dominance of reversing gene expression plasticity-plastic responses that move the levels of gene expression away from the new optima. Nevertheless, evidence from natural populations is still limited.ResultsHere, we studied gene expression plasticity and its evolution in the montane and lowland populations of an elevationally widespread songbird-the Rufous-capped Babbler (Cyanoderma ruficeps)-with reciprocal transplant experiments and transcriptomic analyses; we set common gardens at altitudes close to these populations' native ranges. We confirmed the prevalence of reversing plasticity in genes associated with altitudinal adaptation. Interestingly, we found a positive relationship between magnitude and degree of evolution in gene expression plasticity, which was pertinent to not only adaptation-associated genes but also the whole transcriptomes from multiple tissues. Furthermore, we revealed that genes with weaker expressional interactions with other genes tended to exhibit stronger plasticity and higher degree of plasticity evolution, which explains the positive magnitude-evolution relationship.ConclusionsOur experimental evidence demonstrates that species may initiate their adaptation to new habitats with genes exhibiting strong expression plasticity. We also highlight the role of expression interdependence among genes in regulating the magnitude and evolution of expression plasticity. This study illuminates how the evolution of phenotypic plasticity in gene expression facilitates the adaptation of species to challenging environments in nature.

Project description:The use of multiple pesticides or drugs can lead to a simultaneous selection pressure for resistance alleles at different loci. Models of resistance evolution focus on how this can delay the spread of resistance through a population, but often neglect how this can also reduce the probability that a resistance allele spreads. This neglected factor has been studied in a parallel literature as selective interference. Models of interference use alternative constructions of fitness, where selection coefficients from different loci either add or multiply. Although these are equivalent under weak selection, the two constructions make alternative predictions under the strong selection that characterizes resistance evolution. Here, simulations are used to examine the effects of interference on the probability of fixation and time to fixation of a new and strongly beneficial mutation in the presence of another strongly beneficial allele with variable starting frequency. The results from simulations show a complicated pattern of effects. The key result is that, under multiplicativity, the presence of the strongly beneficial allele leads to a small reduction in the probability of fixation for the new beneficial mutation up to ~10%, and a negligible increase in the average time to fixation up to ~2%, whereas under additivity, the effect is more substantial at up to ~50% for the probability of fixation and ~100% for the average time to fixation. Consequently, the effect of interference is only an important feature of resistance evolution under additivity. Current evidence from studies of experimental evolution provides widespread support for the basic features of additivity, which suggests that interference may afford resistance a different pattern of evolution than other adaptations: rather than the gradual and simultaneous selection of many alleles with small effects, the rapid evolution of resistance may involve the sequential selection of alleles with large effects.

Dataset Information

Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes.

Publications

Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes.

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