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Nolte, V.

Publications and source records attributed to Nolte, V..

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Environmental temperature is a strong driver of subspecies competition in the Drosophila microbiome

Most microbiome research focusses on the taxonomic composition at the species level to understand the impact of environmental factors, but intraspecific diversity has largely been ignored. To address this significant knowledge gap, we took advantage of the simple, culturable microbiome of Drosophila. First, we documented that natural populations of D. simulans harbor three diverged clades of Lactiplantibacillus plantarum, a key nutritional symbiont. We studied the distinct ecological roles of these three clades by exposing flies with their native microbiome to two temperature regimes in the laboratory. Tracking the three clades within the complete Drosophila microbiome over a period of more than 10 years at two temperatures, we identified strikingly distinct dynamics in response to the selection regime. We confirmed the functional differentiation of the three clades using in vitro growth measurements and in vivo mono-association assays. Our results highlight that environmental selection operates at the subspecies level. Therefore, we conclude that the functional diversification of the microbiome can only be understood when intra- and interspecific diversity is considered.

microbiology↗

Purifying Selection Shapes the Dynamics of P-element Invasion in Drosophila Populations

BackgroundTransposable elements (TEs) are DNA sequences that can move within a host genome. Many new TE insertions have deleterious effects on their host and are therefore removed by purifying selection. The genomic distribution of TEs thus reflects a balance between new insertions and purifying selection. However, the inference of purifying selection against deleterious TE insertions from the patterns observed in natural populations is challenged by the confounding effects of demographic events, such as population bottlenecks and migration. ResultsWe used Experimental Evolution to study the role of purifying selection during the invasion of the P-element, a highly invasive TE, in replicated Drosophila simulans populations under controlled laboratory conditions. Because the change in P-element copy number over time provides information about the transposition rate and the effect of purifying selection, we repeatedly sequenced the experimental populations to study the P-element invasion dynamics. Based on the empirical data, we used Gaussian Process surrogate models to efficiently explore the parameter space and identify parameter combinations that best reproduce the experimental P-element invasion trajectories. Assuming that beneficial P-element insertions are negligible, we found that, in our experimental populations, 73% (60.9% - 76.1%) of new P-element insertions are under purifying selection with a mean selection coefficient of -0.056 (-0.060 - -0.042), highlighting the central role of selection in shaping P-element invasion dynamics. ConclusionThis study underscores the power of Experimental Evolution as a tool for studying transposable element invasions and highlights the pivotal role of purifying selection in regulating P-element dynamics.

evolutionary biology↗

Genome-wide selection signatures reveal widespread synergistic effects of culture conditions and temperature stress in Drosophila melanogaster

Experimental evolution combined with whole-genome sequencing is a powerful approach to study the adaptive architecture of selected traits, in particular when replicated experimental populations evolving in opposite selective conditions (e.g. hot vs. cold temperature) are compared. Nevertheless, such comparisons could be affected by environmental effects shared between selective regimes (e.g. laboratory adaptation), which complicate the interpretation of selection signatures. Here, we used an experimental design, which takes advantage of the simplicity of selection signatures from founder populations with reduced variation, to study the fitness consequences of the laboratory environment (culture conditions) at two temperature regimes. After 20 generations of adaptation at 18{degrees}C and 29{degrees}C, strong genome-wide selection signatures were observed. About one third of the selection signatures can be either attributed to temperature effects, laboratory adaptation or the joint effects of both. The fitness consequences reflecting the combined effects of temperature and laboratory adaptation were more extreme in the hot environment for 83% of the affected genomic regions, fitting the pattern of larger expression differences between founders at 29{degrees}C. We propose that evolve and resequence (E&R) with reduced genetic variation allows to study genome-wide fitness consequences driven by the interaction of multiple environmental factors.

evolutionary biology↗

The transposition rate has little influence on equilibrium copy numbers of the P-element

The invasion of transposable elements (TEs) in mammals and invertebrates, is likely stopped by piRNAs that emerge after insertion of the TE into a piRNA cluster (the trap model). It remains, however, still unclear which factors influence the dynamics of TE invasions. The activity of the TE (i.e. transposition rate) is one of the frequently discussed key factors. Here we take advantage of the temperature-dependent activity of the P-element, a widely studied eukaryotic TE, to test how TE activity affects the dynamics of a TE invasion. Taking advantage of the temperature-specific activity of the P-element, we monitored its invasion dynamics in experimental Drosophila simulans populations at hot and cold culture conditions. Despite marked differences in transposition rates, the P-element reached very similar copy numbers at both temperatures. The reduction of the insertion rate upon approaching the copy number plateau was accompanied by the emergence of similar amounts of piRNAs against the P-element at both temperatures. Interestingly, the ping-pong cycle, which degrades TE transcripts, becomes only active after the copy number has reached the plateau. We show that the P-element abundance is an order of magnitude lower and fewer P-element insertions in piRNA clusters were observed than expected under the trap model. We conclude that the transposition rate has at the most only a minor influence on TE abundance, but other factors, such as paramutations or selection against TE insertions are shaping the TE composition of organism.

evolutionary biology↗

Highly parallel genomic selection response in replicated Drosophila melanogaster populations with reduced genetic variation

Many adaptive traits are polygenic and frequently more loci contributing to the phenotype than needed are segregating in populations to express a phenotypic optimum. Experimental evolution provides a powerful approach to study polygenic adaptation using replicated populations adapting to a new controlled environment. Since genetic redundancy often results in non-parallel selection responses among replicates, we propose a modified Evolve and Resequencing (E&R) design that maximizes the similarity among replicates. Rather than starting from many founders, we only use two inbred Drosophila melanogaster strains and expose them to a very extreme, hot temperature environment (29{degrees}C). After 20 generations, we detect many genomic regions with a strong, highly parallel selection response in 10 evolved replicates. The X chromosome has a more pronounced selection response than the autosomes, which may be attributed to dominance effects. Furthermore, we find that the median selection coefficient for all chromosomes is higher in our two-genotype experiment than in classic E&R studies. Since two random genomes harbor sufficient variation for adaptive responses, we propose that this approach is particularly well-suited for the analysis of polygenic adaptation.

evolutionary biology↗

Evolution of phenotypic variance provides insights into the genetic basis of adaption

Most traits are polygenic and the contributing loci can be identified by GWAS. Their adaptive architecture is, however, difficult to characterize. Here, we propose to study the adaptive architecture of traits by monitoring the evolution of their phenotypic variance during adaptation to a new environment in well-defined laboratory conditions. Extensive computer simulations show that the evolution of phenotypic variance in a replicated experimental evolution setting can distinguish between oligogenic and polygenic adaptive architectures. We compared gene expression variance in male Drosophila simulans before and after 100 generations of adaptation to a novel hot environment. The variance change in gene expression was indistinguishable for genes with and without a significant change in mean expression after 100 generations of evolution. We suggest that a majority of adaptive gene expression evolution can be explained by a polygenic architecture. We propose that tracking the evolution of phenotypic variance across generations can provide an approach to characterize the adaptive architecture. Significant StatementIt is widely accepted that most complex traits have a polygenic basis. Nevertheless, it is difficult to predict which of these loci are responding to selection when a population is exposed to a new selection regime. To address this situation, we propose to infer the adaptive architecture for traits by tracking the evolution of their phenotypic variance during adaptation to a new environment. As a case study, we analyze the evolution of gene expression variance in outbred Drosophila simulans populations adapting to a new temperature regime to infer the genetic architecture of adaptive gene expression evolution. We suggested that the adaptive gene expression evolution is better explained by a polygenic architecture.

evolutionary biology↗

The evolution of phenotypic plasticity in response to temperature stress

Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to environmental variation. The importance of phenotypic plasticity in natural populations and its contribution to phenotypic evolution during rapid environmental change is widely debated. Here, we show that thermal plasticity of gene expression in natural populations is a key component of its adaptation: evolution to novel thermal environments increases ancestral plasticity rather than mean genetic expression. We determined the evolution of plasticity in gene expression by conducting laboratory natural selection on a Drosophila simulans population in hot and cold environments. After more than 60 generations in the hot environment, 325 genes evolved a change in plasticity relative to the natural ancestral population. Plasticity increased in 75% of these genes, which were strongly enriched for several well-defined functional categories (e.g. chitin metabolism, glycolysis and oxidative phosphorylation). Furthermore, we show that plasticity in gene expression of populations exposed to different temperatures is rather similar across species. We conclude that most of the ancestral plasticity can evolve further in more extreme environments.

evolutionary biology↗

The adaptive architecture is shaped by population ancestry and not by selection regime

Understanding the genetic architecture of adaptive phenotypes is a key question in evolutionary biology. One particularly promising approach is Evolve and Resequence (E&R), which combines advantages of experimental evolution such as time series, replicate populations and controlled environmental conditions, with whole genome sequencing. The recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures - either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates. Here, we exposed the founder population from Portugal to a cold temperature regime. Although almost no selection targets were shared between the hot and cold selection regime, the adaptive architecture was similar: we identified a moderate number of loci under strong selection (19 selected alleles, mean selection coefficient = 0.072) and very parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime. These observations have a pronounced impact on our understanding of adaptation in natural populations.Competing Interest StatementThe authors have declared no competing interest.View Full Text

evolutionary biology↗

Transcription-coupled repair in Drosophila melanogaster is independent of the mismatch repair pathway

Transcription-coupled repair (TCR) removes base damage on the transcribed strand of a gene to ensure a quick resumption of transcription. Based on the absence of key enzymes for TCR and empirical evidence, TCR was thought to be missing in Drosophila melanogaster. The recent demonstration of TCR in S2 cells raises the question about the involved genes. Since the mismatch repair (MMR) pathway serves a central role in TCR, at least in Escherichia coli, we studied the mutational signatures in flies with a deletion of the MMR gene spellchecker1 (spel1), a MutS homolog. Whole-genome sequencing of mutation accumulation (MA) lines obtained 7,345 new single nucleotide variants (SNVs) and 5,672 short indel mutations, the largest data set from an MA study in D. melanogaster. Based on the observed mutational strand-asymmetries, we conclude that TCR is still active without spel1. The operation of TCR is further confirmed by a negative association between mutation rate and gene expression. Surprisingly, the TCR signatures are detected for introns, but not for exons. We propose that an additional exon-specific repair pathway is masking the signature of TCR. This study presents the first step towards understanding the molecular basis of TCR in Drosophila melanogaster.

molecular biology↗

Secondary evolve and re-sequencing: an experimental confirmation of putative selection targets without phenotyping

Evolve and re-sequencing (E&R) studies investigate the genomic responses of adaptation during experimental evolution. Because replicate populations evolve in the same controlled environment, consistent responses to selection across replicates are frequently used to identify reliable candidate regions that underlie adaptation to a new environment. However, recent work demonstrated that selection signatures can be restricted to one or a few replicate(s) only. These selection signatures frequently have a weak statistical support, and given the difficulties of functional validation, additional evidence is needed before considering them as candidates for functional analysis. Here, we introduce an experimental procedure to validate candidate loci with weak or replicate-specific selection signature(s). Crossing an evolved population from a primary E&R experiment to the ancestral founder population reduces the frequency of candidate alleles that have reached a high frequency. We hypothesize that genuine selection targets will experience a repeatable frequency increase after the mixing with the ancestral founders if they are exposed to the same environment (secondary E&R experiment). Using this approach, we successfully validate two overlapping selection targets, which showed a mutually exclusive selection signature in a primary E&R experiment of Drosophila simulans adapting to a novel temperature regime. We conclude that secondary E&R experiments provide a reliable confirmation of selection signatures that are either not replicated or show only a low statistical significance in a primary E&R experiment. Such experiments are particularly helpful to prioritize candidate loci for time-consuming functional follow-up investigations.

molecular biology↗

Neuronal function and dopamine signaling evolve at high temperature in Drosophila

Introduction Introduction Main Methods Author contributions Competing interest Materials and Correspondence References Adaptation to local environments is a general principle in nature. In the light of the ongoing climatic change, the mechanisms for temperature adaptation are of particular interest1-2. Many essential biological processes are temperature sensitive, and neuronal activity3-7 is a particularly prominent one as it affects essential, fitness-related traits such as behavior and locomotion8. Here, we investigate if temperature stress triggers adaptation of neuronal signaling. We used replicated laboratory evolution experiments with Drosophila simula ...

evolutionary biology↗

DNA motifs are not general predictors of recombination in two Drosophila sister species.

Meiotic recombination is crucial for chromosomal segregation, and facilitates the spread of beneficial and removal of deleterious mutations. Recombination rates frequently vary along chromosomes and Drosophila melanogaster exhibits a remarkable pattern. Recombination rates gradually decrease towards centromeres and telomeres, with dramatic impact on levels of variation in natural populations. Two close sister species, D. simulans and D. mauritiana do not only have higher recombination rates, but also exhibit a much more homogeneous recombination rate that only drops sharply close to centromeres and telomeres. Because certain sequence motifs are associated with recombination rate variation in D. melanogaster, we tested whether the difference in recombination landscape between D. melanogaster and D. simulans can be explained by the genomic distribution of recombination-rate associated sequence motifs. We constructed the first high resolution recombination map for D. simulans, and searched for motifs linked with high recombination in both sister species. We identified five consensus motifs, present in either species. While the association between motif density and recombination is strong and positive in D. melanogaster, the results are equivocal in D. simulans. Despite the strong association in D. melanogaster, we do not find a decreasing density of these repeat motifs towards centromeres and telomeres. We conclude that the density of recombination-associated repeat motifs cannot explain the large-scale recombination landscape in D. melanogaster, nor the differences to D. simulans. The strong association seen for the sequence motifs in D. melanogaster likely reflects their impact influencing local differences in recombination rates along the genome.

genomics↗

Polygenic adaptation fuels genetic redundancy in Drosophila

The genetic architecture of adaptive traits is of key importance to predict evolutionary responses. Most adaptive traits are polygenic - i.e. result from selection on a large number of genetic loci - but most molecularly characterized traits have a simple genetic basis. This discrepancy is best explained by the difficulty in detecting small allele frequency changes across many contributing loci. To resolve this, we use laboratory natural selection, a framework that is powerful enough to detect signatures for selective sweeps and polygenic adaptation. We exposed 10 replicates of a Drosophila simulans population to a new temperature regime and uncovered a polygenic architecture of an adaptive trait with high genetic redundancy among adaptive alleles. We observed convergent phenotypic responses, e.g. fitness, metabolic rate and fat content, and a strong polygenic response (99 selected alleles; mean s=0.061). However, each of these selected alleles increased in frequency only in a subset of the evolving replicates. Our results show that natural D. simulans populations harbor a vast reservoir of adaptive variation facilitating rapid evolutionary responses. The observed genetic redundancy potentiates this genotypic variation through multiple genetic pathways leading to phenotypic convergence. This key property of adaptive alleles requires the modification of testing strategies in natural populations beyond the search for convergence on the molecular level.

evolutionary biology↗

A simple genetic basis of adaptation to a novel thermal environment results in complex metabolic rewiring in Drosophila

Population genetic theory predicts that rapid adaptation is largely driven by complex traits encoded by many loci of small effect. Because large effect loci are quickly fixed in natural populations, they should not contribute much to rapid adaptation. To investigate the genetic architecture of thermal adaptation - a highly complex trait - we performed experimental evolution on a natural Drosophila simulans population. Transcriptome and respiration measurements revealed extensive metabolic rewiring after only [~]60 generations in a hot environment. Analysis of genome-wide polymorphisms identified two interacting selection targets, Sestrin and SNF4A{gamma}, pointing to AMPK, a central metabolic switch, as a key factor for thermal adaptation. Our results demonstrate that large-effect loci segregating at intermediate allele frequencies can allow natural populations to rapidly respond to selection. Because SNF4A{gamma} also exhibits clinal variation in various Drosophila species, we suggest that this large effect polymorphism is maintained by temporal and spatial temperature variation in natural environments.

evolutionary biology↗