Opinion
The Role of Mutation Bias in Adaptive Evolution

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Highlights

Standard evolutionary theory recognizes only one force (natural selection) that can lead to directional evolutionary change towards increased organismal adaptation.

Critics of standard evolutionary theory have argued that mutational bias is an alternative evolutionary process or cause that can increase organismal adaptation independently of natural selection.

We review the theoretical and empirical literature on mutation bias and identify the conditions under which it is likely to be important in adaptive evolution.

Mutation bias is unlikely to play an important role in adaptive evolution, except under conditions of small population sizes and low amounts of standing genetic variation.

Even if novel mutations are random with respect to organismal needs and are mostly deleterious, selection on the phenotypic expression of novel mutations (developmental bias) may cause alignment between mutational variation and the direction of increased fitness and macroevolutionary divergence, creating an illusory impression of adaptive directionality of novel mutations.

Mutational input is the ultimate source of genetic variation, but mutations are not thought to affect the direction of adaptive evolution. Recently, critics of standard evolutionary theory have questioned the random and non-directional nature of mutations, claiming that the mutational process can be adaptive in its own right. We discuss here mutation bias in adaptive evolution. We find little support for mutation bias as an independent force in adaptive evolution, although it can interact with selection under conditions of small population size and when standing genetic variation is limited, entirely consistent with standard evolutionary theory. We further emphasize that natural selection can shape the phenotypic effects of mutations, giving the false impression that directed mutations are driving adaptive evolution.

Section snippets

Mutation as an Evolutionary Process

In recent years, standard evolutionary theory (see Glossary), which has its origin in the modern synthesis, has come under criticism from some biologists and philosophers 1, 2, 3, 4. Critics argue that standard evolutionary theory, with its main reliance on four population genetic processes (mutation, genetic drift, recombination and selection) (Figure 1) [5], fails to provide a complete account of adaptation and phenotypic evolution [2]. Critics further argue that mutation bias and

The Issue of Non-Random Mutation

Critics of standard evolutionary theory have questioned the assumption that mutations are random 2, 3, 4. We clarify here that ‘random’ only means that novel beneficial mutations do not arise at a higher relative frequency as a direct response to current organismal needs [9]. Standard evolutionary theory and the modern synthesis do, however, make the non-controversial prediction that mutations will tend to have more beneficial effects on average in maladapted populations that are far from their

Theoretical Predictions for the Role of Mutation Bias in Neutral and Adaptive Evolution

Heterogeneous mutation rates can arise due to structural constraints across the genome [11] or because of selection [16]. This is recognized in the neutral theory of molecular evolution [11], and is thus part of standard evolutionary theory. Critics of standard evolutionary theory, however, question both the assumption that the origination rate of a beneficial allele does not influence its fixation probability 8, 13 and that fixation probability is under exclusive control of selection [7].

Parallel Genetic Adaptations Is Insufficient Evidence for Mutation Bias

The study of parallel or convergent adaptations can reveal the power of natural selection leading to similar phenotypes and adaptations in similar environments [31]. Parallel phenotypic evolution may (or may not) be caused by parallel genetic changes at the same base positions (i.e., the same mutations), different mutations within the same loci, or mutations at entirely different sets of loci 32, 33. This has stimulated discussions about the relative role of determinism and historical

Transition–Transversion Bias and Other Forms of Mutation Bias in Adaptation

A common argument for mutation bias as a directional evolutionary force is the transition–transversion bias [48]. Stoltzfus and McCandlish [6] compiled a large dataset from several taxa to quantify the role of transition–transversion bias among adaptive substitutions. Because the rate of transition mutations is higher than the rate of transversions, they argued that the former should be over-represented among adaptive substitutions. They found some evidence for such a pattern, and therefore

Alignment between Mutation and Adaptation as a Result of Past Selection

We have argued that mutation bias is unlikely to drive adaptive evolution alone, and particularly not when standing genetic variation is abundant (Box 2). We have also emphasized that genetic parallelism is unlikely to result from mutation bias alone in the absence of any major role for selection in narrowing down the available evolutionary trajectories. A further finding suggestive of prominent roles for mutation bias or developmental bias in adaptive evolution is the observed alignment

Adaptive Directionality and Similarities between Evolution and Learning

Based on the many past unsuccessful attempts to demonstrate any positive directionality of novel mutations on organismal fitness, one would perhaps expect the issue to now have become finally settled. However, recently there has been a new set of theoretical studies based on neural networks and machine learning [67] that claim to demonstrate that evolution might ‘learn’ from past environments and thereby generalize to novel environments [68]. According to these models, novel mutations could

Challenging Historical Narratives about Mutation Bias in the Modern Synthesis and Standard Evolutionary Theory

We question here some historical narratives around the modern synthesis that are sometimes voiced by critics of standard evolutionary theory 2, 3, including those arguing for mutation bias as a novel mechanism that can direct adaptive evolution 8, 13, 73. According to some of these narratives, the modern synthesis exclusively focused on selection as an evolutionary process 2, 3 and only considered standing genetic variation (‘shifting gene frequencies’) [8], while ignoring the role of novel

Environment → Selection ↔ Mutation

Although we argue that mutation bias is unlikely to be a major and independent force in driving convergent evolutionary responses, we suggest that environmental influences on population genetic parameters have been somewhat neglected. Specifically, the interplay between mutation and selection in driving evolutionary divergence should be investigated in more depth. For example, the role of mutation bias versus fixation bias is somewhat paradoxically turned in favor of selection as baseline

Concluding Remarks

We do not deny a role for mutation bias in adaptation in mutation-limited populations 5, 6, but this role is not independent of selection and such evolution is certainly not mutation-driven. We therefore question if mutation bias should be elevated to become a novel cause or evolutionary process, as argued by some authors 7, 73 (see Outstanding Questions). Stochasticity is already well incorporated into standard evolutionary theory, which has moved well beyond panselectionism [5], as

Acknowledgments

The ideas put forward in this paper and the topics discussed emerged from discussions with Troy Day, Magne Friberg, Thomas F. Hansen, Stephen De Lisle, Tobias Uller, and many others who have directly or indirectly influenced our thinking about mutation bias. We thank Martin Lascoux and Claus Rüffler for input to Boxes 1 and 2. Funding for our research has been provided by the Swedish Research Council (VR) to E.I.S. (grant 2016-03356) and D.B. (grant 2015-05223).

Glossary

Correlational selection
a form of selection that operates on character combinations rather than on traits in isolation. Correlational selection is of interest because it can promote and maintain adaptive genetic covariance between traits.
Developmental bias
a summary term for the non-random production of phenotypes from underlying genotypes (e.g., novel mutations) and environmental conditions (i.e., phenotypic plasticity).
Directed mutation
a discredited idea that mutations are not random with

References (93)

  • D. Noble

    Evolution viewed from physics, physiology and medicine

    Interface Focus

    (2017)
  • M. Lynch

    The frailty of adaptive hypotheses for the origins of organismal complexity

    Proc. Natl. Acad. Sci. U.S.A.

    (2007)
  • A. Stoltzfus et al.

    Mutational biases influence parallel adaptation

    Mol. Biol. Evol.

    (2017)
  • L.Y. Yampolsky et al.

    Bias in the introduction of variation as an orienting factor in evolution

    Evol. Dev.

    (2001)
  • A. Stoltzfus

    Mutationism and the dual causation of evolutionary change

    Evol. Dev.

    (2006)
  • D.J. Futuyma

    Evolutionary biology today and the call for an extended synthesis

    Interface Focus

    (2017)
  • P.D. Sniegowski et al.

    Mutation and adaptation: the directed mutation controversy in evolutionary perspective

    Annu. Rev. Ecol. Syst.

    (1995)
  • M. Kimura

    The Neutral Theory of Molecular Evolution

    (1983)
  • M. Lynch

    Mutation accumulation and the extinction of small populations

    Am. Nat.

    (1995)
  • A. Stoltzfus et al.

    Mendelian-mutationism: the forgotten evolutionary synthesis

    J. Hist. Biol.

    (2014)
  • R.A. Fisher

    The Genetical Theory of Natural Selection

    (1930)
  • A. Wagner

    Distributed robustness versus redundancy as causes of mutational robustness

    BioEssays

    (2005)
  • I. Martincorena

    Evidence of non-random mutation rates suggests an evolutionary risk management strategy

    Nature

    (2012)
  • D. Berger

    Temperature effects on life-history trade-offs, germline maintenance and mutation rate under simulated climate warming

    Proc. R. Soc. B.

    (2017)
  • J.B.S. Haldane

    The part played by recurrent mutation in evolution

    Am. Nat.

    (1933)
  • D. Charlesworth

    The sources of adaptive variation

    Proc. Biol. Sci.

    (2017)
  • J. Cairns

    The origin of mutants

    Nature

    (1988)
  • S. Maisnier-Patin et al.

    The origin of mutants under selection: how natural selection mimics mutagenesis (adaptive mutation)

    Cold Spring Harb. Perspect. Biol.

    (2015)
  • D.L. Halligan et al.

    Spontaneous mutation accumulation studies in evolutionary genetics

    Annu. Rev. Ecol. Evol. Syst.

    (2008)
  • T. Bataillon et al.

    Effects of new mutations on fitness: insights from models and data

    Ann. N.Y. Acad. Sci.

    (2014)
  • E. Rajon et al.

    Evolution of molecular error rates and the consequences for evolvability

    Proc. Natl. Acad. Sci.

    (2011)
  • N.P. Sharp et al.

    Evidence for elevated mutation rates in low-quality genotypes

    Proc. Natl. Acad. Sci.

    (2012)
  • A. Pomiankowski

    The evolution of costly mate preferences: I. Fisher and biased mutation

    Evolution

    (1991)
  • L. Rowe et al.

    The lek paradox and the capture of genetic variance by condition dependent traits

    Proc. R. Soc. Lond. Ser. B-Biol. Sci.

    (1996)
  • R.B. Huey

    Rapid evolution of a geographic cline in size in an introduced fly

    Science

    (2000)
  • H.E. Hoekstra et al.

    Different genes underlie adaptive melanism in different populations of rock pocket mice

    Mol. Ecol.

    (2003)
  • N.I. Mundy

    A window on the genetics of evolution: MC1R and plumage colouration in birds

    Proc. Biol. Sci.

    (2005)
  • E.B. Rosenblum

    The molecular basis of phenotypic convergence

    Annu. Rev. Ecol. Evol. Syst.

    (2014)
  • L.-M. Chevin

    Fisher’s model and the genomics of adaptation: restricted pleiotropy, heterogenous mutation, and parallel evolution

    Evolution

    (2010)
  • J.F. Storz

    Causes of molecular convergence and parallelism in protein evolution

    Nat. Rev. Genet.

    (2016)
  • M. Lässig

    Predicting evolution

    Nat. Ecol. Evol.

    (2017)
  • D. Schluter

    Evidence for ecological speciation and its alternative

    Science

    (2009)
  • J.I. Meier

    Ancient hybridization fuels rapid cichlid fish adaptive radiations

    Nat. Commun.

    (2017)
  • G.L. Conte

    The probability of genetic parallelism and convergence in natural populations

    Proc. R. Soc. B

    (2012)
  • H.A. Orr

    The probability of parallel evolution

    Evolution

    (2005)
  • O. Tenaillon

    Tempo and mode of genome evolution in a 50,000-generation experiment

    Nature

    (2016)

    • Cited by (43)

    View all citing articles on Scopus
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