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

Mallard, François; Nolte, Viola; Tobler, Raymond; Kapun, Martin; Schlötterer, Christian

doi:10.1186/s13059-018-1503-4

Cited by 84 publications

(121 citation statements)

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“…While the mean observed selection coefficient depends strongly on the minimum threshold applied to infer selected SNPs, which makes comparisons among studies using different thresholds difficult, the maximal s per REA observed here exceeded those reported for haplotypes in similar studies on Drosophila (Barghi et al, ). This may be the result of the higher number of starting haplotypes (800) and a higher N e in the replicates throughout the experiment (factor 2–4) compared to previous E&R studies with Drosophila (Barghi et al, ; Mallard, Nolte, Tobler, Kapun, & Schlötterer, ; Tobler et al, ), allowing for efficient selection of favourable variants.…”

Section: Discussionmentioning

confidence: 96%

“…This may be the result of the higher number of starting haplotypes (800) and a higher N e in the replicates throughout the experiment (factor 2-4) compared to previous E&R studies with Drosophila (Barghi et al, 2019;Mallard, Nolte, Tobler, Kapun, & Schlötterer, 2018;Tobler et al, 2013), allowing for efficient selection of favourable variants.…”

Section: Pervasive Common Genomic Adaptation Signalmentioning

confidence: 99%

“…Evolve and Resequence (E&R) studies have emerged as useful tool to infer genomic patterns and processes during rapid phenotypic adaptation (Long, Liti, Luptak, & Tenaillon, ; Schlötterer, Kofler, Versace, Tobler, & Franssen, ). To some extent, it even becomes feasible to identify the genomic basis of the experimentally induced phenotypic change in complex multicellular eukaryotes, albeit currently studies with metazoans are restricted to Drosophila (Franssen, Barton, & Schlötterer, ; Michalak, Kang, Schou, Garner, & Loeschcke, ; Mallard, Nolte, Tobler, Kapun, & Schlötterer, ). E&R studies can address fundamental issues in evolutionary biology such as the predictability of evolution (De Visser & Krug, ) and the entwined questions of trait complexity and the mode of their evolution (polygenic adaptation vs. selective sweeps, Stephan, ).…”

Section: Introductionmentioning

confidence: 99%

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Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures

Pfenninger

Foucault

2020

Molecular Ecology

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Evolve and Resquence (E&R) studies are a useful tool to study genomic processes during rapid adaptation, e.g., in the framework of adaptive responses to global climate change. We applied different thermal regimes to a natural Chironomus riparius (Diptera) population in an E&R framework to infer its evolutionary potential for rapid thermal adaptation. We exposed two replicates to three temperatures each (14°C, 20°C and 26°C) for more than two years, the experiment thus lasting 22, 44 or 65 generations, respectively. The two higher temperatures presented a priori moderate, respectively strong selection pressures. Life‐cycle fitness tests revealed no appreciable adaptation to thermal regimes but a common adaptation of all six replicates probably due to the rearing conditions, presumably increased larval density and water quality. Genomic analyses showed a strong, genome‐wide selective response in all replicates (mean s of selected SNPs = 0.305). This genomic response was significantly similar at all genomic levels among all replicates (SNPs, 10 kb windows, genes, exons, regions of elevated allele frequency change [REA]). The intersections among the replicates exposed to the same temperature were either insignificant or underrepresented. This confirmed a selective response to identical selection pressure(s), however, not to thermal regime. Genes closest to the SNP with the highest selection coefficient per REA were enriched for GO terms related to ion transport, regulation of transcription and signal transduction, which supported the presumed acting selection pressures. Our study showed the evolutionary potential for rapid adaptation by genome‐wide and probably polygenic selection on standing genetic variation in C. riparius. However, because of the impossibility to accurately predict the acting selective regime in evolutionary experiments, we discuss the sobering perspectives for inferring the evolutionary potential of natural populations with this approach.

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Section: Discussionmentioning

confidence: 96%

Section: Pervasive Common Genomic Adaptation Signalmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures

Pfenninger

Foucault

2020

Molecular Ecology

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“…Introducing haplovalidate, which reconstructs selected haplotype blocks from genomic E&R time-series data, we provide a tool, to make the reconstruction of selected haplotypes a routine method that does not rely on the availability of haplotype information, neither from the founder population, nor from evolved individuals. Haplovalidate can be applied to a broad range of data, including few selection targets (Mallard et al, 2018) as well as many .…”

Section: Discussionmentioning

confidence: 99%

A generalised approach to detect selected haplotype blocks in Evolve and Resequence experiments

Otte¹,

Schlötterer²

2019

Preprint

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Shifting from the analysis of single nucleotide polymorphisms to the reconstruction of selected haplotypes greatly facilitates the interpretation of Evolve and Resequence (E&R) experiments. Merging highly correlated hitchhiker SNPs into haplotype blocks reduces thousands of candidates to few selected regions. Current methods of haplotype reconstruction from Pool-Seq data need a variety of data-specific parameters that are typically defined ad hoc and require haplotype sequences for validation. Here, we introduce haplovalidate, a tool which detects selected haplotypes in a broad range of Pool-seq time series data without the need of sequenced haplotypes. Haplovalidate makes data-driven choices of two key parameters for the clustering procedure, the minimum correlation between SNPs constituting a cluster and the window size. Applying haplovalidate to simulated and experimental E&R data reliably detects selected haplotype blocks with low false discovery rates -independent if few or many selection targets are included. Our analyses identified an important restriction of the haplotype block-based approach to describe the genomic architecture of adaptation.We detected a substantial fraction of haplotypes containing multiple selection targets. These blocks were considered as one region of selection and therefore led to under-estimation of the number of selection targets. We demonstrate that the separate analysis of earlier time points can significantly increase the separation of selection targets into individual haplotype blocks. We conclude that the analysis of selected haplotype blocks has a large potential for the characterisation of the adaptive architecture with E&R experiments.

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“…Metabolic rewiring is a common response among different organisms to their surrounding environment 1 . Different cell types differ in their preferred mode of metabolism in order to harness energy and generate its required set of metabolites 2–5 .…”

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confidence: 99%

Distinct metabolic states of a cell guide alternate fates of mutational buffering through altered proteostasis

Verma

Saxena

Rajashekar

et al. 2019

Preprint

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15Changes in metabolism can alter the cellular milieu; can this also change intracellular 16 proteostasis? Since proteostasis can modulate mutational buffering, if change in metabolism has 17 the ability to change proteostasis, arguably, it should also alter mutational buffering. Building on 18 this, we find that altered cellular metabolic states in E. coli buffer distinct mutations. mutants had folding problems in vivo and were differently chaperoned in different metabolic 20 states. Notably, this assistance was dependent upon the metabolites and not on the increase in 21 canonical chaperone machineries. Additionally, we were able to reconstitute the folding 22 assistance afforded by metabolites in vitro and propose that changes in metabolite concentrations 23 have the potential to alter proteostasis. Collectively, we unravel that the metabolite pools are 24 bona fide members of proteostasis and aid in mutational buffering. Given the plasticity in 25 cellular metabolism, we posit that metabolic alterations may play an important role in the 26 positive or negative regulation of proteostasis. 27 28 29Metabolic rewiring is a common response among different organisms to their surrounding 30 environment 1 . Different cell types differ in their preferred mode of metabolism in order to 31 harness energy and generate its required set of metabolites [2][3][4][5] . Interestingly, many of the cellular 32 metabolites are known to change protein folding pathways by modifying protein stability and 33 folding kinetics in vitro at high concentrations. Some of the special ones like polyphosphates 6,7 34 and ATP 8,9 are known to affect cellular protein aggregation during certain stresses. It is 35 important to know if the change in metabolite composition of cellular milieu can alter 36 intracellular protein folding capacity. 37If metabolites and metabolism can affect proteostasis it may have two fundamental implications. 38 1) Metabolism-dependent change in proteostasis may aid evolution of the whole proteome when 39 there is a change in an organism's niche or surrounding climate that alters its internal 40 environment, or when an organism undergoes a large change in metabolism 4,10 . For example, 41 some mutations may be rendered inactive in one metabolic state (a metabolic state is defined by 42 the concentration of each of the metabolites the cell accumulates), while being active in a 43 different one. Switching of metabolic niches may expose certain phenotypes that are hidden by 44 metabolism-dependent genetic buffering. 2) tissue-specific metabolic differences may predispose 45 cell-types to aggregate or misfold particular mutant protein, even while the protein is 46 ubiquitously expressed. Age-dependent change in metabolism may also render certain tissues 47 more prone to age-dependent aggregation 11,12 . This may have implications in explaining the late-48 onset tissue specificity of aggregation associated disorders 13 which has been hard to explain with 49 our current understanding of proteostasis components. 5...

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

Cited by 84 publications

References 80 publications

Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures

Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures

A generalised approach to detect selected haplotype blocks in Evolve and Resequence experiments

Distinct metabolic states of a cell guide alternate fates of mutational buffering through altered proteostasis

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