A theory of oligogenic adaptation of a quantitative trait

Höllinger, Ilse; Wölfl, Benjamin; Hermisson, Joachim

doi:10.1093/genetics/iyad139

Cited by 8 publications

(9 citation statements)

References 71 publications

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“…Nevertheless, they find that their population-scaled background mutation rate Θ bg , which corresponds closely to our 2Θ, explains the main differences in the patterns of adaptation, i.e., few sweeps versus many slight shifts. This main conclusion is confirmed by Höllinger et al (2023) for an additive trait subject to a sudden shift in the optimum phenotype, again for equal mutation effects.…”

Section: Discussionmentioning

confidence: 57%

“…Other studies focused on polygenic adaptation under directional selection (Höllinger et al, 2019), for instance caused by a sudden big environmental shift (Thornton, 2019, Höllinger et al, 2023). Although the assumptions on the genetic architecture and on the form of directional selection differ among these studies, they show that selective sweeps at several loci (parallel or successive) occur more often than in the above discussed scenario.…”

Section: Introductionmentioning

confidence: 99%

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Polygenic dynamics underlying the response of quantitative traits to directional selection

Götsch¹,

Bürger²

2023

Preprint

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We study the response of a quantitative trait to exponential directional selection in a finite haploid population, both on the genetic and the phenotypic level. We assume an infinite sites model, in which the number of new mutations per generation in the population follows a Poisson distribution (with mean Θ) and each mutation occurs at a new, previously monomorphic site. Mutation effects are beneficial and drawn from a distribution. Sites are unlinked and contribute additively to the trait. Assuming that selection is stronger than random genetic drift, we model the initial phase of the dynamics by a slightly supercritical Galton-Watson process. This enables us to obtain time-dependent results. We show that the copy-number distribution of the mutant in generation n, conditioned on survival until n, is described accurately by the deterministic increase from an initial distribution with mean 1. This distribution corresponds to the absolutely continuous part W+ of the random variable, typically denoted W, that characterizes the stochasticity accumulating during the mutant's sweep. In bypassing, we prove the folklore result that W+ is approximately exponentially distributed, but in general not exactly so by deriving its second and third moment. A proper transformation yields the approximate mutant frequency dynamics in a Wright-Fisher population of size N. Then we derive explicitly the (approximate) time dependence of the expected mean and variance of the trait and of the expected number of segregating sites. Unexpectedly, we obtain highly accurate expressions even for the quasi-stationary phase, when the expected per-generation response has equilibrated. These refine classical results, and they are derived from first principles. We find that Θ is the main determinant of the pattern of adaptation at the genetic level, i.e., whether the response is mainly due to sweeps or to small allele-frequency shifts, and the number of segregating sites is an appropriate indicator for it. The selection strength determines primarily the rate of adaptation. The accuracy of our results is tested for a Poisson offspring distribution by comprehensive simulations in a Wright-Fisher framework.

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Section: Discussionmentioning

confidence: 57%

Section: Introductionmentioning

confidence: 99%

Polygenic dynamics underlying the response of quantitative traits to directional selection

Götsch¹,

Bürger²

2023

Preprint

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“…4). This demonstrates the oligogenic architecture of adaptive tracking in the system is resilient to perturbations of background/starting allele frequencies, likely a result of the additivity of the marginal effects of alleles underpinning the evolving traits and the very strong selective pressures in the system (71).…”

Section: Discussionmentioning

confidence: 91%

Continuously fluctuating selection reveals extreme granularity and parallelism of adaptive tracking

Bitter,

Berardi,

Oken

et al. 2023

Preprint

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Temporally fluctuating environmental conditions are a ubiquitous feature of natural habitats. Yet, how finely natural populations adaptively track fluctuating selection pressures via shifts in standing genetic variation is unknown. We generated high-frequency, genome-wide allele frequency data from a genetically diverse population of Drosophila melanogaster in extensively replicated field mesocosms from late June to mid-December, a period of ~12 generations. Adaptation throughout the fundamental ecological phases of population expansion, peak density, and collapse was underpinned by extremely rapid, parallel changes in genomic variation across replicates. Yet, the dominant direction of selection fluctuated repeatedly, even within each of these ecological phases. Comparing patterns of allele frequency change to an independent dataset procured from the same experimental system demonstrated that the targets of selection are predictable across years. In concert, our results reveal fitness-relevance of standing variation that is likely to be masked by inference approaches based on static population sampling, or insufficiently resolved time-series data. We propose such fine-scaled temporally fluctuating selection may be an important force maintaining functional genetic variation in natural populations and an important stochastic force affecting levels of standing genetic variation genome-wide.

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“…In a theoretical analysis of polygenic adaptation, Höllinger et al . (2019) showed that this level of mutation input will lead to polygenic adaptation via subtle frequency shifts; it has subsequently been shown that this condition holds generally across different fitness models Höllinger et al . (2023); Götsch and Bürger (2023).…”

Section: Methodsmentioning

confidence: 99%

“…2018; Thornton 2019) or new analytical developments (Jain and Stephan 2017a,b; Höllinger et al . 2019; Hayward and Sella 2022; Höllinger et al . 2023; Götsch and Bürger 2023).…”

Section: Introductionmentioning

confidence: 99%

Polygenic selection to a changing optimum under self–fertilisation

Hartfield

Glémin

2022

Preprint

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Many traits are polygenic, affected by multiple genetic variants throughout the genome. Selection acting on these traits involves co–ordinated allele– frequency changes at these underlying variants, and this process has been extensively studied in random–mating populations. Yet many species self– fertilise to some degree, which incurs changes to genetic diversity, recombination and genome segregation. These factors cumulatively influence how polygenic selection is realised in nature. Here, we use simulations to investigate to what extent self–fertilisation affects polygenic adaptation to a new environment. We find that self–fertilisation can incur a fitness advantage through purging maladaptive genotypes. While the degree of self– fertilisation has little influence on how quickly a population adapts to a new optimum, those with the highest long–term fitness tended to have high levels of selfing (at least 90%). Very high levels of self–fertilisation (99% and above) causes fixation of variants with compensatory effects in elevated linkage disequilibrium across the genome. Conversely, if mutations are pleiotropic then only a few major–effect variants fix along with many neutral hitchhikers, with a transient increase in linkage disequilibrium. If deleterious mutations are also present then linkage–block formation is disrupted in highly–selfing species, with fewer mutations contributing to adaptation and less chance of high–linkage genomes persisting over time. We also show how these outcomes differ in outcrossing populations with rescaled mutation and recombination rates, demonstrating that elevated homozygosity also influences the selection response. These results show potential advantages to self–fertilisation when adapting to a new environment, and how the mating system affects the genetic composition of polygenic selection.Website for simulation codehttps://github.com/MattHartfield/Polygenic-Selfing

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A theory of oligogenic adaptation of a quantitative trait

Cited by 8 publications

References 71 publications

Polygenic dynamics underlying the response of quantitative traits to directional selection

Polygenic dynamics underlying the response of quantitative traits to directional selection

Continuously fluctuating selection reveals extreme granularity and parallelism of adaptive tracking

Polygenic selection to a changing optimum under self–fertilisation

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