Fluctuating selection and the determinants of genetic variation

Johnson, O.; Tobler, Raymond; Schmidt, Joshua

doi:10.1016/j.tig.2023.02.004

Cited by 19 publications

(14 citation statements)

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“…Despite the breadth of theoretical research, until recently, the general consensus held that temporally fluctuating selection was comparatively ineffective at maintaining genetic variation compared to spatially varying selection and other negative frequency‐dependent selection mechanisms (Hedrick, 2006). However, more and more studies over the past two decades suggest that temporally fluctuating selection can greatly contribute to the maintenance of genetic variation (Bell, 2010; Johnson et al, 2023; Messer et al, 2016). Indeed, many SNPs in the Drosophila genome show persistent seasonal fluctuations (Bergland et al, 2014; Machado et al, 2021; Rudman et al, 2022) and genotype frequencies of Daphnia change in response to seasonal food availability (Schaffner et al, 2019).…”

Section: Theories In Population Geneticsmentioning

confidence: 99%

“…More recently, an increasing number of empirical studies have demonstrated that temporally fluctuating selection/environments are important in maintaining both genetic variation (Bergland et al, 2014; Machado et al, 2021; Rudman et al, 2022; Yi & Dean, 2013) and species diversity (Angert et al, 2009; Ellner et al, 2019; Hallett et al, 2019; Letten et al, 2018; Sommer, 1985; Zepeda & Martorell, 2019). Although the topic itself has a long history in ecology (reviewed in Barabás et al, 2018; Chesson, 2000b; Ellner et al, 2019; Stump & Vasseur, 2023; Yamamichi & Letten, 2022)and evolutionary biology (reviewed in Felsenstein, 1976; Frank, 2011; Gillespie, 1991; Hedrick, 1986; Hedrick, 2006; Hedrick et al, 1976; Johnson et al, 2023: see also Figure 1 and Figure S1), the recent accumulation of empirical evidence has coincided with renewed theoretical interest into the role of temporally fluctuating environments in maintaining genetic variation (Bertram & Masel, 2019b; Dean, 2018; Dean et al, 2017; Gulisija et al, 2016; Kim, 2023; Novak & Barton, 2017; Park & Kim, 2019; Schreiber, 2020; Svardal et al, 2015; Wittmann et al, 2017, 2023; Yamamichi et al, 2019; Yamamichi & Hoso, 2017) and species diversity (Barabás et al, 2018; Chesson, 2018; Ellner et al, 2019; Fung et al, 2022; Johnson & Hastings, 2022a, 2022b; Meyer et al, 2022; Pande et al, 2020; Schreiber, 2021, 2022; Schreiber et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Eco‐evolutionary maintenance of diversity in fluctuating environments

Yamamichi,

Letten,

Schreiber

2023

Ecology Letters

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Growing evidence suggests that temporally fluctuating environments are important in maintaining variation both within and between species. To date, however, studies of genetic variation within a population have been largely conducted by evolutionary biologists (particularly population geneticists), while population and community ecologists have concentrated more on diversity at the species level. Despite considerable conceptual overlap, the commonalities and differences of these two alternative paradigms have yet to come under close scrutiny. Here, we review theoretical and empirical studies in population genetics and community ecology focusing on the ‘temporal storage effect’ and synthesise theories of diversity maintenance across different levels of biological organisation. Drawing on Chesson's coexistence theory, we explain how temporally fluctuating environments promote the maintenance of genetic variation and species diversity. We propose a further synthesis of the two disciplines by comparing models employing traditional frequency‐dependent dynamics and those adopting density‐dependent dynamics. We then address how temporal fluctuations promote genetic and species diversity simultaneously via rapid evolution and eco‐evolutionary dynamics. Comparing and synthesising ecological and evolutionary approaches will accelerate our understanding of diversity maintenance in nature.

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Section: Theories In Population Geneticsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Eco‐evolutionary maintenance of diversity in fluctuating environments

Yamamichi,

Letten,

Schreiber

2023

Ecology Letters

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“…This temporal selection can occur in regular cycles due to changing seasons or other environmental variables with regular, repeating patterns or it can shift more irregularly over time, both of which can under certain circumstances lead to the long‐term maintenance of variation (Bell, 2010; Gillespie, 1978; Pfenninger & Foucault, 2022; Wittmann et al, 2017). In the latter case, rapid adaptation via repeated, aperiodic shifts in allele frequency can occur in response to non‐cyclic environmental changes (Bell, 2010; Pfenninger & Foucault, 2022); while, in the former case, rapid, repeated, cyclic shifts in allele frequency can occur in response to periodically changing environmental conditions, such as seasons, if the selected alleles are sufficiently dominant (Wittmann et al, 2017; reviewed in Johnson et al, 2023). It should be noted, however, that theoretical studies have suggested that temporally fluctuating selection can also decrease polymorphism in unlinked, non‐selected regions (Park & Kim, 2019; Taylor, 2013; Wittmann et al, 2023).…”

Section: Allele Frequency Shifts and The Long‐term Maintenance Of Gen...mentioning

confidence: 99%

“…Such resources allow us to directly track evolution over time, including the response to natural environmental fluctuations, which can provide insights into the tempo and dynamics of evolution and adaptation. Indeed, a growing number of studies in various species have leveraged this type of population time series data to characterize genetic variation and evolution in natural populations over time (Mathieson et al, 2015; Hofmanová et al, 2016; Castañeda‐Rico et al, 2020; Machado et al, 2021; Lange et al, 2022; Pfenninger & Foucault, 2022; reviewed in Johnson et al, 2023).…”

Section: Allele Frequency Variation and Dynamics In Natural Drosophil...mentioning

confidence: 99%

Rapid evolutionary change, constraints and the maintenance of polymorphism in natural populations of Drosophila melanogaster

2023

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Allele frequencies can shift rapidly within natural populations. Under certain conditions, repeated rapid allele frequency shifts can lead to the long‐term maintenance of polymorphism. In recent years, studies of the model insect Drosophila melanogaster have suggested that this phenomenon is more common than previously believed and is often driven by some form of balancing selection, such as temporally fluctuating or sexually antagonistic selection. Here we discuss some of the general insights into rapid evolutionary change revealed by large‐scale population genomic studies, as well as the functional and mechanistic causes of rapid adaptation uncovered by single‐gene studies. As an example of the latter, we consider a regulatory polymorphism of the D. melanogaster fezzik gene. Polymorphism at this site has been maintained at intermediate frequency over an extended period of time. Regular observations from a single population over a period of 7 years revealed significant differences in the frequency of the derived allele and its variance across collections between the sexes. These patterns are highly unlikely to arise from genetic drift alone or from the action of sexually antagonistic or temporally fluctuating selection individually. Instead, the joint action of sexually antagonistic and temporally fluctuating selection can best explain the observed rapid and repeated allele frequency shifts. Temporal studies such as those reviewed here further our understanding of how rapid changes in selection can lead to the long‐term maintenance of polymorphism as well as improve our knowledge of the forces driving and limiting adaptation in nature.

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“…Based on models for other types of genetic variation (see e.g. Haldane and Jayakar 1963; Hedrick 1976; Johnson et al . 2023; Wittmann et al .…”

Section: Introductionmentioning

confidence: 99%

How does plant chemodiversity evolve? Testing five hypotheses in one population genetic model

Wittmann,

Bräutigam

2024

Preprint

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Plant chemodiversity, the diversity of plant specialized metabolites, is an important dimension of biodiversity. However, there are so far few quantitative models to test verbal hypotheses on how chemodiversity evolved. Here we develop such a model to test predictions of five hypotheses: the "fluctuating selection hypothesis", the "dominance reversal hypothesis", the interaction diversity hypothesis, the synergy hypothesis, and the screening hypothesis. We build a population genetic model of a plant population attacked by herbivore species whose occurrence fluctuates over time. We study the model using mathematical analysis and individual-based simulations. As predicted by the "dominance reversal hypothesis", chemodiversity can be maintained if alleles conferring a defense metabolite are dominant with respect to the benefits, but recessive with respect to costs. However, even smaller changes in dominance can maintain polymorphism. Moreover, our results underpin and elaborate predictions of the synergy and interaction diversity hypotheses, and, to the extent that our model can address it, the screening hypotheses. By contrast, we found only partial support for the "fluctuating selection hypothesis". In summary, we have developed a flexible model and tested various verbal models for the evolution of chemodiversity. Next, more mechanistic models are needed that explicitly consider the organization of metabolic pathways.

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Fluctuating selection and the determinants of genetic variation

Cited by 19 publications

References 99 publications

Eco‐evolutionary maintenance of diversity in fluctuating environments

Eco‐evolutionary maintenance of diversity in fluctuating environments

Rapid evolutionary change, constraints and the maintenance of polymorphism in natural populations of Drosophila melanogaster

How does plant chemodiversity evolve? Testing five hypotheses in one population genetic model

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