Constructive Neutral Evolution 20 Years Later

AbstractEvolution has led to a great diversity that ranges from elegant simplicity to ornate complexity. Many complex features are often assumed to be more functional or adaptive than their simpler alternatives. However, in 1999, Arlin Stolzfus published a paper in the Journal of Molecular Evolution that outlined a framework in which complexity can arise through a series of non-adaptive steps. He called this framework Constructive Neutral Evolution (CNE). Despite its two-decade-old roots, many evolutionary biologists still appear to be unaware of this explanatory framework for the origins of complexity. In this perspective piece, we explain the theory of CNE and how it changes the order of events in narratives that describe the evolution of complexity. We also provide an extensive list of cellular features that may have become more complex through CNE. We end by discussing strategies to determine whether complexity arose through neutral or adaptive processes.

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The generality of Constructive Neutral Evolution

Biology & Philosophy ◽

10.1007/s10539-018-9614-6 ◽

2018 ◽

Vol 33 (1-2) ◽

Cited By ~ 6

Author(s):

T. D. P. Brunet ◽

W. Ford Doolittle

Keyword(s):

Neutral Evolution ◽

Constructive Neutral Evolution

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Combining molecular evolution and environmental genomics to unravel adaptive processes of MHC class IIB diversity in European minnows (Phoxinus phoxinus)

Ecology and Evolution ◽

10.1002/ece3.650 ◽

2013 ◽

Vol 3 (8) ◽

pp. 2568-2585 ◽

Cited By ~ 9

Author(s):

Helene Collin ◽

Reto Burri ◽

Fabien Comtesse ◽

Luca Fumagalli

Keyword(s):

Molecular Evolution ◽

Phoxinus Phoxinus ◽

Environmental Genomics ◽

Adaptive Processes ◽

Mhc Class Iib ◽

Class Iib

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Constructive neutral evolution cannot explain current kinetoplastid panediting patterns

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0909867107 ◽

2010 ◽

Vol 107 (7) ◽

pp. E25-E25 ◽

Cited By ~ 10

Author(s):

D. Speijer

Keyword(s):

Neutral Evolution ◽

Constructive Neutral Evolution

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Constructive neutral evolution: exploring evolutionary theory’s curious disconnect

Biology Direct ◽

10.1186/1745-6150-7-35 ◽

2012 ◽

Vol 7 (1) ◽

pp. 35 ◽

Cited By ~ 45

Author(s):

Arlin Stoltzfus

Keyword(s):

Neutral Evolution ◽

Constructive Neutral Evolution

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The Rate of Molecular Evolution When Mutation May Not Be Weak

10.1101/259507 ◽

2018 ◽

Cited By ~ 2

Author(s):

A.P. Jason de Koning ◽

Bianca D. De Sanctis

Keyword(s):

Natural Selection ◽

Molecular Evolution ◽

Population Size ◽

Mutation Rate ◽

Molecular Clock ◽

Neutral Theory ◽

Neutral Evolution ◽

Systematic Bias ◽

Effective Population ◽

Sequence Comparisons

AbstractOne of the most fundamental rules of molecular evolution is that the rate of neutral evolution equals the mutation rate and is independent of effective population size. This result lies at the heart of the Neutral Theory, and is the basis for numerous analytic approaches that are widely applied to infer the action of natural selection across the genome and through time, and for dating divergence events using the molecular clock. However, this result was derived under the assumption that evolution is strongly mutation-limited, and it has not been known whether it generalizes across the range of mutation pressures or the spectrum of mutation types observed in natural populations. Validated by both simulations and exact computational analyses, we present a direct and transparent theoretical analysis of the Wright-Fisher model of population genetics, which shows that some of the most important rules of molecular evolution are fundamentally changed by considering recurrent mutation’s full effect. Surprisingly, the rate of the neutral molecular clock is found to have population-size dependence and to not equal the mutation rate in general. This is because, for increasing values of the population mutation rate parameter (θ), the time spent waiting for mutations quickly becomes smaller than the cumulative time mutants spend segregating before a substitution, resulting in a net deceleration compared to classical theory that depends on the population mutation rate. Furthermore, selection exacerbates this effect such that more adaptive alleles experience a greater deceleration than less adaptive alleles, introducing systematic bias in a wide variety of methods for inferring the strength and direction of natural selection from across-species sequence comparisons. Critically, the classical weak mutation approximation performs well only when θ< 0.1, a threshold that many biological populations seem to exceed.

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THE SELECTIVE VALUE OF ALLELES UNDERLYING POLYGENIC TRAITS

Genetics ◽

10.1093/genetics/108.4.1021 ◽

1984 ◽

Vol 108 (4) ◽

pp. 1021-1033

Author(s):

Michael Lynch

Keyword(s):

Molecular Evolution ◽

Genetic Drift ◽

Genetic Variance ◽

Neutral Theory ◽

Mechanistic Explanation ◽

Neutral Evolution ◽

Stabilizing Selection ◽

Average Effect ◽

Absolute Value ◽

The Mean

ABSTRACT To define the genetic and ecological circumstances that are conductive to evolution via genetic drift at the allelic level, the selection coefficient for a constituent allele of arbitrary effect is derived for a polygenic character exposed to stabilizing selection. Under virtually all possible conditions, alleles within the class for which the absolute value of the average effect is <10-2 phenotypic standard deviations are neutral with respect to each other. In addition, when the mean phenotype is at the optimum and the genetic variance is in selection-drift-mutation equilibrium, a considerable amount of neutral evolution is expected in the class of alleles with intermediate effects on the phenotype. These results help clarify how molecular evolution via genetic drift may occur at a locus despite intense selection and provide a potential mechanistic explanation for the neutral theory of molecular evolution.

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Molecular Evolution of the Avian CHD1 Genes on the Z and W Sex Chromosomes

Genetics ◽

10.1093/genetics/155.4.1903 ◽

2000 ◽

Vol 155 (4) ◽

pp. 1903-1912 ◽

Cited By ~ 2

Author(s):

Anna-Karin Fridolfsson ◽

Hans Ellegren

Keyword(s):

Molecular Evolution ◽

Sex Chromosomes ◽

Sequence Data ◽

Neutral Evolution ◽

Z Chromosome ◽

W Chromosome ◽

Effective Population ◽

Synonymous Substitutions ◽

Nonsynonymous Substitutions ◽

Female Specific

Abstract Genes shared between the nonrecombining parts of the two types of sex chromosomes offer a potential means to study the molecular evolution of the same gene exposed to different genomic environments. We have analyzed the molecular evolution of the coding sequence of the first pair of genes found to be shared by the avian Z (present in both sexes) and W (female-specific) sex chromosomes, CHD1Z and CHD1W. We show here that these two genes evolve independently but are highly conserved at nucleotide as well as amino acid levels, thus not indicating a female-specific role of the CHD1W gene. From comparisons of sequence data from three avian lineages, the frequency of nonsynonymous substitutions (Ka) was found to be higher for CHD1W (1.55 per 100 sites) than for CHD1Z (0.81), while the opposite was found for synonymous substitutions (Ks, 13.5 vs. 22.7). We argue that the lower effective population size and the absence of recombination on the W chromosome will generally imply that nonsynonymous substitutions accumulate faster on this chromosome than on the Z chromosome. The same should be true for the Y chromosome relative to the X chromosome in XY systems. Our data are compatible with a male-biased mutation rate, manifested by the faster rate of neutral evolution (synonymous substitutions) on the Z chromosome than on the female-specific W chromosome.

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