Polygenic adaptation: a unifying framework to understand positive selection

Abstract

Most adaption processes have a polygenic genetic basis, but even with the recent explosive growth of genomic data we are still lacking a unified framework describing the dynamics of selected alleles. Building on recent theoretical and empirical work we introduce the concept of adaptive architecture, which extends the genetic architecture of an adaptive trait by factors influencing its adaptive potential and population genetic principles. Because adaptation can be typically achieved by many different combinations of adaptive alleles (redundancy), we describe how two characteristics — heterogeneity among loci and non-parallelism between replicated populations — are hallmarks for the characterization of polygenic adaptation in evolving populations. We discuss how this unified framework can be applied to natural and experimental populations.

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Fig. 1: Alternative adaptive paradigms: selective sweeps versus the infinitesimal model.
Fig. 2: Different approaches to characterize polygenic adaptation.
Fig. 3: Genetic redundancy and heterogeneity among loci are the main characteristics of polygenic adaptation.
Fig. 4: Different stages of polygenic adaptation.

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Acknowledgements

C.S. and J.H. are supported by various Austrian Science Fund (FWF) grants (W-1225-B20, P27630-B20, P29133-B29). Thanks to S. Allen, N. Barton, S.-K. Hsu, R. Kofler and T. MacKay for discussion and feedback on earlier versions of the manuscript.

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Correspondence to Joachim Hermisson or Christian Schlötterer.

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Supplementary information

Glossary

Adaptive architecture

The measure of the probability that alleles contribute to adaptation. Adaptive architecture extends the genetic architecture by including further factors that influence the adaptive potential.

Adaptive introgression

New, favourable alleles are introduced into a population by migration.

Admixture graph

A representation of the divergence and admixture between populations.

Clines

Spatial patterns of allele frequency differences, which are maintained by a spatial selection gradient.

Common garden experiments

Experiments that, in order to control for the effects of the environment on phenotypes, measure the phenotypes of different genotypes in the same/similar environments.

Epistasis

Interaction between genes in a non-additive way.

Genetic architecture

Information about genes, with their associated effect sizes and patterns of pleiotropy, epistasis and dominance.

Genetic basis

The set of all loci contributing to a trait, but without reference to effect sizes or pleiotropy, epistasis or dominance.

Genetic drift

A stochastic process arising from the random sampling of gametes contributing to the next generation. In small populations, genetic drift can be strong and results in large, non-directional allele frequency changes.

Genome-wide association studies

(GWAS). A genetic technique that identifies statistically significant associations between phenotypes and underlying genetic variants. GWAS are particularly powerful, because they take advantage of recombination events that occurred historically in the focal population.

Infinitesimal model

The phenotype is determined by a very large (infinite) number of alleles, each with a very small effect, and by the environment.

Mutation–selection balance

An equilibrium situation for a population close to an adaptive optimum. The same number of new deleterious alleles are introduced into the population by mutation as are removed by purifying selection.

Non-synonymous SNPs

Single-nucleotide polymorphisms (SNPs) in protein-coding genes that result in an amino acid replacement.

Parallelism

(Also known as convergence or repeatability). Replicate populations reach the same trait values using the same set of alleles; non-parallelism is the possible consequence of redundancy. Parallelism has been also described for asexual microorganisms, where the same mutations are independently acquired in replicate populations.

Pleiotropy

A single gene affects multiple traits.

Polygenic traits

(Also known as complex traits). Quantitatively variable phenotypes that are affected by many contributing loci and the environment.

Purifying selection

Removal of deleterious alleles from a population.

Quantitative trait locus (QTL) mapping

A genetic mapping technique that relies on recombination events that occurred during the experiment.

Quantitative traits

Traits with a continuous distribution of phenotypes with a large number of contributing alleles.

Redundancy

Different combinations of alleles produce the same phenotypic value.

Selective sweeps

Classic selection signatures in molecular population genetics describing a pattern of reduced DNA polymorphism around the site of a recently fixed beneficial allele.

Singleton density score

A test statistic to detect selection based on the distance of singleton single-nucleotide polymorphisms nearest to the focal variant.

Soft sweeps

Different alleles at the same locus are favoured and contribute to adaptation. They can either be generated by recurrent mutations or they segregate in the population before the adaptive episode starts.

Stabilizing selection

Selection favours individuals with an intermediate trait value.

Standing genetic variation

Polymorphic sites segregating in a natural population.

Swamping

Beneficial alleles are driven to extinction by immigration of non-favoured alleles.

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Barghi, N., Hermisson, J. & Schlötterer, C. Polygenic adaptation: a unifying framework to understand positive selection. Nat Rev Genet (2020). https://doi.org/10.1038/s41576-020-0250-z

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