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The genetic theory of adaptation: a brief history

Nature Reviews Genetics volume 6, pages 119127 (2005) | Download Citation

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Abstract

Theoretical studies of adaptation have exploded over the past decade. This work has been inspired by recent, surprising findings in the experimental study of adaptation. For example, morphological evolution sometimes involves a modest number of genetic changes, with some individual changes having a large effect on the phenotype or fitness. Here I survey the history of adaptation theory, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation. I also discuss the challenges that face contemporary theories of adaptation.

Key points

  • Early evolutionists believed that the genetic basis of adaptation was micromutational.

  • This view was supported by Ronald Fisher's classical mathematical analysis (of 1930) of his 'geometric model' of adaptation.

  • Beginning in the 1980s, studies of quantitative trait loci and microbial experimental evolution revealed that adaptation sometimes involves a modest number of genes, some of which have surprisingly large effects. These experimental findings pose a serious challenge to evolutionary theory.

  • So far, phenotype-based and DNA sequence-based models of adaptation have yielded surprisingly similar results, indicating the possibility of a robust theory of adaptation.

  • Phenotypic models of adaptation show that the genes that cause adaptation should have approximately exponentially distributed effects; that is, involve many genes that have small effect and a few genes that have large effect.

  • DNA sequence models of adaptation indicate that adaptation should involve mutations of relatively large fitness effects and that adaptation is characterized by a pattern of diminishing returns, in which early substitutions have large fitness effects and later ones have smaller effects.

  • Current theories of adaptation adequately explain certain qualitative patterns that characterize genetic data on adaptation; however, it is not yet clear if these theories can explain these data quantitatively.

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Acknowledgements

This work was supported by a grant from the US National Institutes of Health.

Author information

Affiliations

  1. Department of Biology, University of Rochester, Rochester, New York 14627, USA.  aorr@mail.rochester.edu

    • H. Allen Orr

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Competing interests

The author declares no competing financial interests.

Glossary

STANDING GENETIC VARIATION

Allelic variation that is currently segregating within a population; as opposed to alleles that appear by new mutation events.

FITNESS

A quantity that is proportional to the mean number of viable, fertile progeny produced by a genotype.

DEFICIENCY MAPPING

A type of genetic mapping that uses chromosomal deletions to 'uncover' recessive alleles that affect a trait.

COMPLEMENTATION TESTS

The use of genetically defined knockout mutations to identify loci that affect a trait.

BIOMETRIC

An approach to the study of phenotypes that emphasizes quantitative measurements (such as of body size) and statistical analysis.

CONTINUOUS CHARACTER

A trait (such as body size) that varies smoothly (continuously) in magnitude; as opposed to discrete characters.

EPISTATIC INTERACTION

Any non-additive interaction between two or more mutations at different loci, such that their combined effect on a phenotype deviates from the sum of their individual effects.

ADDITIVE GENETIC VARIANCE

The part of the total genetic variation that is due to the main (or additive) effects of alleles on a phenotype; as opposed to the dominance and epistatic variances. The additive variance determines the degree of resemblance between relatives and therefore the response to selection.

QUANTITATIVE TRAIT LOCUS

(QTL). A mapped chromosomal region that has a detectable effect on a phenotypic difference between two populations or species. A QTL does not necessarily correspond to a single gene, but can reflect several linked genes.

MICROBIAL EXPERIMENTAL EVOLUTION

An experimental approach that involves the 'real time' adaptation of microbes (typically bacteria, phage or yeast) to defined laboratory conditions.

COMPENSATORY EVOLUTION

Evolution in which a second substitution compensates for the deleterious effects of an earlier substitution.

MUTATION LOAD

The decrease in population fitness below its ideal value owing to recurrent deleterious mutation.

MODULARITY

The idea that organisms are broken developmentally into roughly independent modules, such that mutations affecting traits in one module do not affect traits in other modules.

SHIFTING BALANCE THEORY

A largely verbal theory of evolution which maintains that the interaction between natural selection, genetic drift and migration is more important that the action of any single force. Sewall Wright argued that this theory helped to explain how species could effectively search for the global, and not merely local, optimum.

AFFINITY MATURATION

An increase in the affinity of an antibody for an antigen which is seen as an immune response improves.

SPIN GLASSES

Magnetic objects that are disordered and in which adjacent dipoles can either 'point' in the same direction or in opposite directions.

MOLECULAR CLOCK

The empirical finding that a particular type of protein or DNA sequence evolves at a nearly constant rate through time.

POISSON PROCESS

A simple statistical process in which there is a small and constant probability of change during each short interval of time.

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https://doi.org/10.1038/nrg1523