Adaptive Evolution Of Gene Expression Research Articles

Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora

Phenotypic plasticity in ancestral populations is hypothesized to facilitate adaptation, but evidence is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel adaptive changes has not been explored. The most general finding is that ancestral responses to a new environment are reversed following adaptation (known as reversion). We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared with zinc-sensitive plants. We show that ancestral plasticity that moves expression closer to the optimum value in the new environment influences the evolution of gene expression among genes that are likely to be involved in adaptation and increases the chance that genes are recruited repeatedly during adaptation. However, despite convergence in gene expression levels between independently adapted lineages, ancestral plasticity does not influence how similar expression values of adaptive genes become. Surprisingly, we also observed that ancestral plasticity that increases fitness often becomes genetically determined and fixed, that is, genetically assimilated. These results emphasize the important role of ancestral plasticity in parallel adaptation.

An incoherent feedforward loop facilitates adaptive tuning of gene expression.

We studied adaptive evolution of gene expression using long-term experimental evolution of Saccharomyces cerevisiae in ammonium-limited chemostats. We found repeated selection for non-synonymous variation in the DNA binding domain of the transcriptional activator, GAT1, which functions with the repressor, DAL80 in an incoherent type-1 feedforward loop (I1-FFL) to control expression of the high affinity ammonium transporter gene, MEP2. Missense mutations in the DNA binding domain of GAT1 reduce its binding to the GATAA consensus sequence. However, we show experimentally, and using mathematical modeling, that decreases in GAT1 binding result in increased expression of MEP2 as a consequence of properties of I1-FFLs. Our results show that I1-FFLs, one of the most commonly occurring network motifs in transcriptional networks, can facilitate adaptive tuning of gene expression through modulation of transcription factor binding affinities. Our findings highlight the importance of gene regulatory architectures in the evolution of gene expression.

Erratum: Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature.

This corrects the article DOI: 10.1038/nature15256.

Adaptive Evolution of Gene Expression in Drosophila

Gene expression levels are important quantitative traits that link genotypes to molecular functions and fitness. In Drosophila, population-genetic studies have revealed substantial adaptive evolution at the genomic level, but the evolutionary modes of gene expression remain controversial. Here, we present evidence that adaptation dominates the evolution of gene expression levels in flies. We show that 64% of the observed expression divergence across seven Drosophila species are adaptive changes driven by directional selection. Our results are derived from time-resolved data of gene expression divergence across a family of related species, using a probabilistic inference method for gene-specific selection. Adaptive gene expression is stronger in specific functional classes, including regulation, sensory perception, sexual behavior, and morphology. Moreover, we identify a large group of genes with sex-specific adaptation of expression, which predominantly occurs in males. Our analysis opens an avenue to map system-wide selection on molecular quantitative traits independently of their genetic basis.

Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature.

Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.

Divergence in cis-regulatory sequences surrounding the opsin gene arrays of African cichlid fishes

BackgroundDivergence within cis-regulatory sequences may contribute to the adaptive evolution of gene expression, but functional alleles in these regions are difficult to identify without abundant genomic resources. Among African cichlid fishes, the differential expression of seven opsin genes has produced adaptive differences in visual sensitivity. Quantitative genetic analysis suggests that cis-regulatory alleles near the SWS2-LWS opsins may contribute to this variation. Here, we sequence BACs containing the opsin genes of two cichlids, Oreochromis niloticus and Metriaclima zebra. We use phylogenetic footprinting and shadowing to examine divergence in conserved non-coding elements, promoter sequences, and 3'-UTRs surrounding each opsin in search of candidate cis-regulatory sequences that influence cichlid opsin expression.ResultsWe identified 20 conserved non-coding elements surrounding the opsins of cichlids and other teleosts, including one known enhancer and a retinal microRNA. Most conserved elements contained computationally-predicted binding sites that correspond to transcription factors that function in vertebrate opsin expression; O. niloticus and M. zebra were significantly divergent in two of these. Similarly, we found a large number of relevant transcription factor binding sites within each opsin's proximal promoter, and identified five opsins that were considerably divergent in both expression and the number of transcription factor binding sites shared between O. niloticus and M. zebra. We also found several microRNA target sites within the 3'-UTR of each opsin, including two 3'-UTRs that differ significantly between O. niloticus and M. zebra. Finally, we examined interspecific divergence among 18 phenotypically diverse cichlids from Lake Malawi for one conserved non-coding element, two 3'-UTRs, and five opsin proximal promoters. We found that all regions were highly conserved with some evidence of CRX transcription factor binding site turnover. We also found three SNPs within two opsin promoters and one non-coding element that had weak association with cichlid opsin expression.ConclusionsThis study is the first to systematically search the opsins of cichlids for putative cis-regulatory sequences. Although many putative regulatory regions are highly conserved across a large number of phenotypically diverse cichlids, we found at least nine divergent sequences that could contribute to opsin expression differences in cis and stand out as candidates for future functional analyses.

Reply to Jensen and Rando: Population size change does not account for widespread gene expression adaptation in yeast

We recently reported evidence for widespread adaptive evolution of gene expression in budding yeast (1). One component of our analysis was the demonstration that genes we predicted (based on gene expression data) to have undergone positive selection showed reduced heterozygosity compared with a control set, suggesting the action of recent selective sweeps. Jensen and Rando (2) propose that this result is because of “a failure to consider the demographic history of these strains.” However, this claim is not supported either by theory or empirical evidence.

Evidence for widespread adaptive evolution of gene expression in budding yeast

Changes in gene expression have been proposed to underlie many, or even most, adaptive differences between species. Despite the increasing acceptance of this view, only a handful of cases of adaptive gene expression evolution have been demonstrated. To address this discrepancy, we introduce a simple test for lineage-specific selection on gene expression. Applying the test to genome-wide gene expression data from the budding yeast Saccharomyces cerevisiae, we find that hundreds of gene expression levels have been subject to lineage-specific selection. Comparing these findings with independent population genetic evidence of selective sweeps suggests that this lineage-specific selection has resulted in recent sweeps at over a hundred genes, most of which led to increased transcript levels. Examination of the implicated genes revealed a specific biochemical pathway--ergosterol biosynthesis--where the expression of multiple genes has been subject to selection for reduced levels. In sum, these results suggest that adaptive evolution of gene expression is common in yeast, that regulatory adaptation can occur at the level of entire pathways, and that similar genome-wide scans may be possible in other species, including humans.

Adaptive Evolution of Gene Expression in Antarctic Fishes: Divergent Transcription of the 5′-to-5′ Linked Adult α1- and β-Globin Genes of the Antarctic TeleostNotothenia coriicepsis Controlled by Dual Promoters and Intergenic Enhancers1

Unlike temperate fishes, Antarctic fishes of the notothenioid suborder, whose body temperatures (−2 to 1°C) conform to the Southern Ocean, must express their genomes in an extremely cold thermal regime. To determine whether these fishes have evolved compensatory adjustments that maintain efficient gene transcription at low temperatures, we have initiated studies of the cis-acting regulatory elements that control globin gene expression in the Antarctic rockcod Notothenia coriiceps and in its close relative, the temperate New Zealand black cod N. angustata (habitat temperature = 6 to 15°C). The genes encoding the major α1 and β globins of these fishes are tightly linked in head-to-head (5′ to 5′) orientation. The intergenic regions separating the globin genes in the two fishes, ∼4.3 kb in N. coriiceps and ∼3.2 kb in N. angustata, are highly similar in sequence, the major difference being the absence of a 1.1-kb, repeat-containing segment in the latter. To assess the promoter and enhancer activities of the intergenic regions, each was cloned into the luciferase-reporter vector pGL3-Basic, and the constructs were transfected into MEL cells. Upon DMSO induction of MEL cell differentiation, each of the α/β-intergenic regions functioned in both orientations as erythroid-responsive transcriptional regulators. However, expression of luciferase mediated by the N. coriiceps intergene was 6-fold greater in the α orientation than that for the N. angustata intergene and 2-fold greater for the β. The greater transcription-stimulating activity of the N. coriiceps intergene can be attributed to two enhancers composed of combinations of CAC/Sp1 and GATA motifs and located in direct repeat elements. N. angustata, which lacked repetitive structure in its intergene, contained a single copy of the enhancer. We propose that cold adaptation of globin gene expression in N. coriiceps evolved in part through duplication and refinement of critical cis-acting regulatory elements as the Southern Ocean cooled during the past 25 million years.

Adaptive Evolution of Gene Expression in Antarctic Fishes: Divergent Transcription of the 5′-to-5′ Linked Adult α1- and β-Globin Genes of the Antarctic TeleostNotothenia coriicepsis Controlled by Dual Promoters and Intergenic Enhancers

Unlike temperate fishes, Antarctic fishes of the notothenioid suborder, whose body temperatures (−2 to +1°C) conform to the Southern Ocean, must express their genomes in an extremely cold thermal regime. To determine whether these fishes have evolved compensatory adjustments that maintain efficient gene transcription at low temperatures, we have initiated studies of the cis-acting regulatory elements that control globin gene expression in the Antarctic rockcod Notothenia coriiceps and in its close relative, the temperate New Zealand black cod N. angustata (habitat temperature = +6 to +15°C). The genes encoding the major α1 and β globins of these fishes are tightly linked in head-to-head (5′ to 5′) orientation. The intergenic regions separating the globin genes in the two fishes, ∼4.3 kb in N. coriiceps and ∼3.2 kb in N. angustata, are highly similar in sequence, the major difference being the absence of a 1.1-kb, repeat-containing segment in the latter. To assess the promoter and enhancer activities of the intergenic regions, each was cloned into the luciferase-reporter vector pGL3-Basic, and the constructs were transfected into MEL cells. Upon DMSO induction of MEL cell differentiation, each of the α/β-intergenic regions functioned in both orientations as erythroid-responsive transcriptional regulators. However, expression of luciferase mediated by the N. coriiceps intergene was 6-fold greater in the α orientation than that for the N. angustata intergene and 2-fold greater for the β. The greater transcription-stimulating activity of the N. coriiceps intergene can be attributed to two enhancers composed of combinations of CAC/Sp1 and GATA motifs and located in direct repeat elements. N. angustata, which lacked repetitive structure in its intergene, contained a single copy of the enhancer. We propose that cold adaptation of globin gene expression in N. coriiceps evolved in part through duplication and refinement of critical cis-acting regulatory elements as the Southern Ocean cooled during the past 25 million years.