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Ecological genomics of local adaptation

Nature Reviews Genetics volume 14, pages 807–820 (2013)Cite this article

Subjects

Key Points

  • The study of local adaptation is often focused on polygenic traits and requires the estimation of fitness in the field — both aspects pose many challenges.

  • Reciprocal transplant experiments are the 'gold standard' for local adaptation studies. These are not often possible, but good surrogate approaches can be found in other types of common environmental experiments.

  • Until now, the genetic basis of local adaptation has been studied in traits with simple inheritance and in model organisms with well-developed genomic resources.

  • The end results of selection for adaptation to specific environmental conditions can be studied in isolated populations, in the framework that is designed for those conditions.

  • If the process of local adaptation owing to migration–selection balance is to be studied, then populations that are connected by ongoing gene flow need to be studied.

  • Most plant studies suggest that the majority of polygenic adaptive traits are influenced by many loci with small effects, with contributions from only a few loci with larger effects. In forest trees, hardly any large-effect loci have been detected.

  • Most animal studies have concentrated on adaptation based on distinct phenotypic polymorphisms, with monogenic or oligogenic inheritance. Genetic variation in polygenic traits has been less studied, but results on human height, for example, suggest small effects in many loci.

  • Combining different phenotype and population genetics approaches using an explicit theoretical framework can provide strong total evidence even if individual methods are not conclusive, for example, when identifying loci under selection.

Abstract

It is increasingly important to improve our understanding of the genetic basis of local adaptation because of its relevance to climate change, crop and animal production, and conservation of genetic resources. Phenotypic patterns that are generated by spatially varying selection have long been observed, and both genetic mapping and field experiments provided initial insights into the genetic architecture of adaptive traits. Genomic tools are now allowing genome-wide studies, and recent theoretical advances can help to design research strategies that combine genomics and field experiments to examine the genetics of local adaptation. These advances are also allowing research in non-model species, the adaptation patterns of which may differ from those of traditional model species.

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Figure 1: Defining local adaptation.
Figure 2: Effect sizes of alleles from association or QTL mapping studies.
Figure 3: Evidence for local adaptation in lateral plate numbers in three-spined sticklebacks using different approaches.

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Acknowledgements

The authors thank P. Leinonen for comments on the manuscript. O.S. is supported by the Academy of Finland (Grant number 132611) and the ProCoGen FP7 EU project; M.L. by the Swedish Research Council, Erik Philip-Sörensen Fund and BioDiversa (Linktree and Tiptree projects); and J.M. by the Academy of Finland (Grant number 252597).

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Authors and Affiliations

  1. Department of Biology and Biocenter Oulu, University of Oulu, Oulu, FIN-90014, Finland

    Outi Savolainen

  2. Department of Ecology and Genetics, Evolutionary Biology Center, University of Uppsala, Uppsala, SE-75236, Sweden

    Martin Lascoux

  3. Department of Biosciences, Ecological Genetics Research Unit, University of Helsinki, Helsinki, FI-00014, Finland

    Juha Merilä

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  1. Outi Savolainen
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Correspondence to Outi Savolainen.

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PowerPoint slides

Glossary

Fitness

The contribution of the genes of an individual to the next generation, usually approximated through measuring survival and reproductive success.

Phenology

The timing of life history events, such as the start of growth or flowering in plants or the arrival to breeding grounds by birds.

Adaptive plasticity

The phenomenon by which a genotype can result in alternative phenotypes in different environments so that the overall fitness of the genotype is increased.

Deterministic model

A model in which the same starting conditions result in the same outcome, as opposed to stochastic models in which chance effects influence the results.

Effect size

The contribution of a locus or an allele to phenotypic variance in a trait.

Clines

The gradual phenotypic or allele frequency changes along a geographical or environmental gradient.

Resequencing

A method to obtain population data by sequencing multiple individuals of a species that has already had a reference genome sequenced.

Parallel evolution

The repeated and independent evolution of similar adaptations (phenotypic or molecular) in multiple populations.

Migration–selection balance

The phenomenon in which the relative strengths of migration and selection determine the level of polymorphism.

Conditional neutrality

A situation in which some alleles may be advantageous in one environment but neutral in other environments.

Reciprocal transplant experiments

Field experiments in which individuals from at least two populations are reared in their respective native and non-native environments.

Stabilizing selection

A situation in which phenotypes that are close to an optimum have highest fitness.

Infinitesimal model

A model in which variation in a quantitative trait is assumed to be due to small effects at many loci.

Quantitative trait locus

(QTL). A genomic area that is found to be associated with variation in a quantitative trait in the progeny of a genetic cross.

Recombinant inbred lines

(RILs). Lines generated by first crossing differentiated parents to produce heterozygous offspring that are self-fertilized. After a few generations, the self-fertilized lines contain different mixtures of parental genomes in a homozygous state.

Inbreeding depression

The decreased fitness of progeny owing to mating between relatives.

Linkage disequilibrium

(LD). The nonrandom association of alleles at two or more different loci.

Antagonistic pleiotropy

The phenomenon in which alternative alleles at a given locus are favoured in different environments.

Polygenic traits

Traits that are influenced by variation at many loci.

Quantitative trait nucleotides

(QTNs). The causative nucleotides that govern the expression of variation in given traits.

Hudson–Kreitman–Aguadé tests

(HKA tests). Tests of selection versus neutrality, based on the comparison of divergence between species with diversity within species between different genomic areas.

Selective sweeps

When a mutation with a beneficial fitness effect arises in a population, natural selection will rapidly increase the frequency of the mutation to a high frequency (partial sweep) or to fixation (complete sweep), which results in a reduction of diversity at and around the selected locus.

Wright fixation index

(FST). The proportion of the total genetic variability that occurs among populations. It is typically used as a measure of the level of population genetic differentiation.

FST–QST comparisons

Tests for selection that compare the degree of differentiation in quantitative traits (QST) with the population genetic differentiation at the marker loci (FST).

Standing genetic variation

Existing variation in a population as opposed to variation that is emerging owing to mutation.

Restriction-site-associated DNA sequencing

(RAD–seq). A technique for partial DNA sequencing, in which DNA is first cut with restriction enzymes and the DNA next to these sites is then sequenced.

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Savolainen, O., Lascoux, M. & Merilä, J. Ecological genomics of local adaptation. Nat Rev Genet 14, 807–820 (2013). https://doi.org/10.1038/nrg3522

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