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Adaptive evolution: evaluating empirical support for theoretical predictions

Key Points

  • The emergence and evolutionary fate of an adaptive allele depends on three broad theoretical principles: the initial frequency of the allele when it becomes favoured by selection; the strength of selection on the adaptive allele; and the effective size and demography of the population in which it arises.

  • Adaptive alleles may originate from de novo mutations at high risk of elimination by genetic drift or from previously neutral or nearly neutral alleles segregating at intermediate frequency when they become advantageous. Alternatively, adaptation may occur through subtle frequency changes in many loci controlling a trait.

  • The strength of selection on an allele depends on its cumulative effects on the target trait and on unrelated beneficial or deleterious traits. These effect sizes are determined by the trait's genetic architecture, the allele's position in its regulatory or biochemical network, environmental influences and genetic background.

  • Larger populations sample more potentially adaptive mutations and are less likely to lose adaptive alleles to genetic drift, even when selection is weak. Migration between populations in contrasting environments introduces new genetic variation that may either encourage or prevent local adaptation.

  • Recent empirical work integrating functional genetics and genomics with evolutionary biology has both conformed to and conflicted with expectations from first principles. Resolution of these discrepancies will require a deeper, more nuanced understanding of molecular and population genetic processes.

  • More poorly understood factors, such as agents and mechanisms of selection, phenotypic plasticity, gene-by-environment interactions and environmental variability, are major challenges for evolutionary biologists.

Abstract

Adaptive evolution is shaped by the interaction of population genetics, natural selection and underlying network and biochemical constraints. Variation created by mutation, the raw material for evolutionary change, is translated into phenotypes by flux through metabolic pathways and by the topography and dynamics of molecular networks. Finally, the retention of genetic variation and the efficacy of selection depend on population genetics and demographic history. Emergent high-throughput experimental methods and sequencing technologies allow us to gather more evidence and to move beyond the theory in different systems and populations. Here we review the extent to which recent evidence supports long-established theoretical principles of adaptation.

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Figure 1: Determinants of fixation of adaptive alleles.
Figure 2: Genetic architecture of human height.
Figure 3: Importance of network effects for adaptation.
Figure 4: Hypothetical mutational trajectories.
Figure 5: The dual nature of recombination.

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Acknowledgements

We thank J. T. Anderson, D. Lowry, P. Magwene, A. Schmid and three anonymous reviewers for helpful discussion and comments. We also acknowledge the authors of the many excellent studies that could not be included in this Review owing to space limitations. This work was supported by the US National Institutes of Health (award R01 GM086496 to T.M.-O.; training grant 5T32GM007754-32 to the Duke University Program in Genetics and Genomics) and the US National Science Foundation (award EF-0723447 to T.M.-O.; dissertation grant 1110445 to C.F.O.-M.).

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Correspondence to Thomas Mitchell-Olds.

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Glossary

Effective population size

(Ne). The size of an ideal population that would experience genetic drift at the same rate as the actual population.

Selection coefficient

The proportional change in fitness owing to a mutation.

Genetic architecture

Also called trait architecture, this is a summary of the allelic effects and frequencies of the genes underlying a given phenotypic trait and their emergent properties, such as epistasis, pleiotropy and modularity.

Introgression

The introduction of a gene into a population or species by crossing with a different population or species.

Major genes

Phenotypic differences between alleles at a locus can range from large phenotypic effects (major genes) to small effects (minor genes). A major gene at intermediate frequency will control a fairly large proportion of trait variation but would have little effect on variation when rare.

Connectivity

A gene's degree of connectivity is the number of direct links to or from other genes in its network.

Centrality

Sometimes referred to as 'between-ness', a gene's degree of centrality is the number of shortest paths between pairs of other genes that must pass through it.

Pleiotropy

The control of multiple traits by a single locus.

Adaptive landscape

A conceptual surface that describes the fitness of all possible genotypic combinations of an organism.

Epistasis

Interaction between genes. The dependence of the effect of a mutation on other sites in the same gene or in other loci, resulting in non-additive effects on phenotype.

Sign epistasis

Epistatic interactions for which the phenotypic effect of a mutation has a different sign in different genetic backgrounds.

Negative epistasis

Epistatic interactions that lessen the magnitude of trait changes, such that combined effects of beneficial mutations are less than their individual effects.

Background selection

The purging of non-deleterious alleles that are closely linked to deleterious sites.

Mullerian mimicry

When two or more poisonous species mimic each other's warning signals for shared predators.

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Olson-Manning, C., Wagner, M. & Mitchell-Olds, T. Adaptive evolution: evaluating empirical support for theoretical predictions. Nat Rev Genet 13, 867–877 (2012). https://doi.org/10.1038/nrg3322

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