Elucidating the molecular architecture of adaptation via evolve and resequence experiments

Long, Anthony D.; Liti, Gianni; Lupták, Andrej; Tenaillon, Olivier

doi:10.1038/nrg3937

Cited by 226 publications

(248 citation statements)

References 148 publications

(201 reference statements)

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“…Gene or chromosomal region amplification and aneuploidy are also molecular mechanisms that have been described as fast and easy short-term adaptive solutions. They may allow a population to survive or grow in response to sudden abrupt change but may be too costly to prevail in the long term [5,22,87]. One can imagine that these simple adaptive changes will be replaced by more refined regulatory mechanisms in the long term.…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

“…Their short generation time and generally small genome sizes allow evolution to be followed over relatively short periods of time in the wild and in the laboratory, for instance through the use of genetic engineering or experimental evolution. The combination of experimental evolution and whole-genome resequencing has greatly accelerated our understanding of how organisms respond to selection [5][6][7][8]. Most importantly, these experiments have allowed the identification of the molecular changes that may increase organismal fitness when the environment is changing.…”

Section: Introductionmentioning

confidence: 99%

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Molecular and cellular bases of adaptation to a changing environment in microorganisms

Bleuven

Landry

2016

Proc. R. Soc. B.

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Environmental heterogeneity constitutes an evolutionary challenge for organisms. While evolutionary dynamics under variable conditions has been explored for decades, we still know relatively little about the cellular and molecular mechanisms involved. It is of paramount importance to examine these molecular bases because they may play an important role in shaping the course of evolution. In this review, we examine the diversity of adaptive mechanisms in the face of environmental changes. We exploit the recent literature on microbial systems because those have benefited the most from the recent emergence of genetic engineering and experimental evolution followed by genome sequencing. We identify four emerging trends: (i) an adaptive molecular change in a pathway often results in fitness trade-off in alternative environments but the effects are dependent on a mutation's genetic background; (ii) adaptive changes often modify transcriptional and signalling pathways; (iii) several adaptive changes may occur within the same molecular pathway but be associated with pleiotropy of different signs across environments; (iv) because of their large associated costs, macromolecular changes such as gene amplification and aneuploidy may be a rapid mechanism of adaptation in the short-term only. The course of adaptation in a variable environment, therefore, depends on the complexity of the environment but also on the molecular relationships among the genes involved and between the genes and the phenotypes under selection.

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Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Molecular and cellular bases of adaptation to a changing environment in microorganisms

Bleuven

Landry

2016

Proc. R. Soc. B.

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“…URING experimental evolution studies, populations are maintained under specific laboratory conditions (Kawecki et al 2012;Long et al 2015;Schlötterer et al 2015). In sexually reproducing organisms, the census population size is typically kept fixed at fairly low numbers, rarely exceeding 2000 individuals.…”

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confidence: 99%

Estimating effective population size from temporal allele frequency changes in experimental evolution

Jónás¹,

Taus²,

Kosiol³

et al. 2016

Preprint

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The effective population size (N e ) is a major factor determining allele frequency changes in natural and experimental populations. Temporal methods provide a powerful and simple approach to estimate short-term N e : They use allele frequency shifts between temporal samples to calculate the standardized variance, which is directly related to N e : Here we focus on experimental evolution studies that often rely on repeated sequencing of samples in pools (Pool-seq). Pool-seq is cost-effective and often outperforms individual-based sequencing in estimating allele frequencies, but it is associated with atypical sampling properties: Additional to sampling individuals, sequencing DNA in pools leads to a second round of sampling, which increases the variance of allele frequency estimates. We propose a new estimator of N e ; which relies on allele frequency changes in temporal data and corrects for the variance in both sampling steps. In simulations, we obtain accurate N e estimates, as long as the drift variance is not too small compared to the sampling and sequencing variance. In addition to genome-wide N e estimates, we extend our method using a recursive partitioning approach to estimate N e locally along the chromosome. Since the type I error is controlled, our method permits the identification of genomic regions that differ significantly in their N e estimates. We present an application to Pool-seq data from experimental evolution with Drosophila and provide recommendations for whole-genome data. The estimator is computationally efficient and available as an R package at https://github.com/ThomasTaus/Nest. KEYWORDS effective population size; genetic drift; Pool-seq; experimental evolution D URING experimental evolution studies, populations are maintained under specific laboratory conditions (Kawecki et al. 2012;Long et al. 2015;Schlötterer et al. 2015). In sexually reproducing organisms, the census population size is typically kept fixed at fairly low numbers, rarely exceeding 2000 individuals. With such small population sizes, genetic drift causes stochastic fluctuations in allele frequencies. Under neutrality, the level of random frequency changes is determined by the effective population size (N e ) (Wright 1931). Furthermore, the efficacy of selection is influenced by N e : For weakly selected alleles, the probability of fixation is directly proportional to the product of N e and the intensity of selection (Fisher 1930;Kimura 1964). As changes in allele frequency are greatly affected by the population size, it is fundamental to estimate N e accurately to understand molecular variation in experimental evolution studies. Krimbas and Tsakas (1971) estimated N e using the standardized variance of allele frequency (F, see also Falconer and Mackay 1996) from longitudinal samples in natural populations of olive flies. As F was calculated from these samples, they accounted for the sampling variance that also contributed to the true allele frequency variance. This approach was further improved and used by sev...

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“…More practically, EE has been used to understand and prevent the evolution of antibiotic resistance in microbes (Palmer & Kishony 2013). Importantly, the recent decline in the costs of sequencing have allowed an extension of the EE approach, termed "evolve and resequence" (E and R) to address the genomic changes underlying adaptation (Long et al 2015). E and R provides a more ecologically relevant complement to mutant studies, by revealing the actual genes and pathways accessible to evolution in natural populations.…”

Section: Approaches To Studying Life Historiesmentioning

confidence: 99%

“…It seems unlikely that no changes in fecundity have evolved, and the transition from poor larval food conditions to the control diet in combination with early reproduction requires particular further attention as the most likely place in which trade-offs may be involved. Furthermore, as mentioned in the introduction, evolve and resequence (E&R) approaches allow the identification of the pathways and processes accessible to evolution in natural populations Long et al 2015). An exciting future direction that is ongoing is to apply E&R to these populations in order to identify the underlying genomic changes involved in mediating the phenotypic changes.…”

Section: Larval Dietmentioning

confidence: 99%

Linking growing up and getting old : plastic and evolutionary effects of developmental diet on adult phenotypes and gene expression in the fruit fly

May¹

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Elucidating the molecular architecture of adaptation via evolve and resequence experiments

Cited by 226 publications

References 148 publications

Molecular and cellular bases of adaptation to a changing environment in microorganisms

Molecular and cellular bases of adaptation to a changing environment in microorganisms

Estimating effective population size from temporal allele frequency changes in experimental evolution

Linking growing up and getting old : plastic and evolutionary effects of developmental diet on adult phenotypes and gene expression in the fruit fly

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