Epistasis as a Source of Increased Additive Genetic Variance at Population Bottlenecks

Cheverud, James M.; Routman, Eric J.

doi:10.2307/2410645

Cited by 142 publications

(166 citation statements)

References 0 publications

Supporting

Mentioning

163

Contrasting

Order By: Relevance

“…Mayr (23) criticized the supposed neglect of epistasis by "bean-bag genetics," provoking a robust defense by Haldane (24). More recently, it has been proposed that epistatic variance can be "converted" into additive variance following a bottleneck, aiding adaptation (25). The failure of large genome-wide association studies to assign much heritable variance to specific loci (the so-called "missing heritability") has been attributed to epistasis (26,27), although this explanation is unnecessary (28).…”

Section: Discussionmentioning

confidence: 99%

The effect of gene interactions on the long-term response to selection

Paixão

Barton

2016

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

View full text Add to dashboard Cite

The role of gene interactions in the evolutionary process has long been controversial. Although some argue that they are not of importance, because most variation is additive, others claim that their effect in the long term can be substantial. Here, we focus on the long-term effects of genetic interactions under directional selection assuming no mutation or dominance, and that epistasis is symmetrical overall. We ask by how much the mean of a complex trait can be increased by selection and analyze two extreme regimes, in which either drift or selection dominate the dynamics of allele frequencies. In both scenarios, epistatic interactions affect the long-term response to selection by modulating the additive genetic variance. When drift dominates, we extend Robertson's [Robertson A (1960) Proc R Soc Lond B Biol Sci 153(951):234−249] argument to show that, for any form of epistasis, the total response of a haploid population is proportional to the initial total genotypic variance. In contrast, the total response of a diploid population is increased by epistasis, for a given initial genotypic variance. When selection dominates, we show that the total selection response can only be increased by epistasis when some initially deleterious alleles become favored as the genetic background changes. We find a simple approximation for this effect and show that, in this regime, it is the structure of the genotype−phenotype map that matters and not the variance components of the population.T he relation between an organism's genotype and its phenotype is immensely complicated, yet quantitative genetics predicts the correlations between relatives, and the response to selection over tens of generations, based primarily on an additive model. How do interactions between genes affect the response to selection? This question is not easy to answer: Although the additive model can be represented by a few parameters, there are an enormous number of possible relationships between genotype and phenotype. Some insight may come from studying specific well-understood systems, for example, regulation of gene expression by binding of transcription factors, or folding of RNA molecules. Here, we take the alternative approach, seeking statistical regularities, while making minimal assumptions about the nature of epistasis.There has been a long-standing debate about the effect of genetic interactions on adaptation (1-7). Although some claim that they are unimportant because they contribute very little to the total genetic variance of a population, and consequently to its short-term response, others claim that their long-term effects can be substantial. At the heart of the debate is the distinction between what has been called physiological and statistical epistasis. The former is independent of the state of the population, whereas the latter is the statistical contribution of gene interactions to the trait variance, which depends on the allele frequencies (8, 9).In the absence of new mutations, the total response to selection is limited by the in...

show abstract

Section: Discussionmentioning

confidence: 99%

The effect of gene interactions on the long-term response to selection

Paixão

Barton

2016

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

View full text Add to dashboard Cite

show abstract

“…This finding is reminiscent of results obtained by Doebley et al (1995), which indicates that two QTLs affecting plant architecture and inflorescence structure have tremendously different effects in a maize or teosinte (wild progenitor of maize) background. The importance of genetic background effects and epistatic relationships among new combination of genes has been documented (Matzke et al, 1993;Pooni et al, 1994;Cheverud and Routman, 1995;Doebley et al, 1995;Cheverud and Routman, 1996;Eshed and Zamir, 1996;Routman and Cheverud, 1997).…”

Section: Discussionmentioning

confidence: 99%

Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana

Syed

Chen

2004

Heredity

View full text Add to dashboard Cite

The underlying mechanisms for hybrid vigor or heterosis are elusive. Here we report a population of recombinant inbred lines (RILs), derived from the two ecotypes, Col and Ler, which can serve as a permanent resource for studying the molecular basis of hybrid vigor in Arabidopsis. Using a North Carolina mating design III (NCIII), we determined the additive and dominant nature of gene action in this population. We detected heterosis among crosses of RILs with one of the two parents (Col and Ler) and analyzed genotypes and heterozygosities for RILs and test cross families (RILs crossed to Col and Ler) using a total of 446 published molecular markers. The performance of RILs and additive and dominant components in the test cross families were used to analyze QTLs for 16 traits, using QTL cartographer and composite interval mapping with 1,000 permutations for each trait. Our data suggest that locus-specific and/or genome-wide differential heterozygosity, including epistasis, plays an important role in the generation of the observed heterosis. Furthermore, the hybrid vigor occurred between two closely related ecotypes, and provides a general mechanism for novel variation generated between genetically similar materials. Heredity (2005) 94, 295-304.

show abstract

“…Selection in this model arises from the assumption that the A and B loci interact to affect fitness. I use the "classic" model of additive-by-additive interactions (45,46), which is a simple model of two-locus fitness effects that favors coadaptation, where certain allelic combinations at the interacting loci are favored and other combinations are disfavored. This form of interaction is particularly useful in examining the evolutionary dynamics of imprinting because it does not include any dominance effects.…”

Section: Modelmentioning

confidence: 99%

Evolution of genomic imprinting as a coordinator of coadapted gene expression

Wolf

2013

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

View full text Add to dashboard Cite

Genomic imprinting is an epigenetic phenomenon in which the expression of a gene copy inherited from the mother differs from that of the copy inherited from the father. Many imprinted genes appear to be highly interconnected through interactions mediated by proteins, RNA, and DNA. These kinds of interactions often favor the evolution of genetic coadaptation, where beneficially interacting alleles evolve to become coinherited. Here I demonstrate theoretically that the presence of gene interactions that favor coadaptation can also favor the evolution of genomic imprinting. Selection favors genomic imprinting because it coordinates the coexpression of positively interacting alleles at different loci. Evolution is expected to proceed through a scenario where selection builds associations between beneficial combinations of alleles and, if one locus evolves to become imprinted, it leads to selection for its interacting partners to match its pattern of imprinting. This process should favor the evolution of physical linkage between interacting genes and therefore may help explain why imprinted genes tend to be found in clusters. The model suggests that, whereas some genes are expected to evolve their imprinting status because selection directly favors a specific pattern of parent-of-origin-dependent expression, other genes may evolve imprinting as a coevolutionary response to match the expression pattern of their interacting partners. As a result, some genes will show phenotypic effects consistent with the predictions of models for the evolution of genomic imprinting (e.g., conflict models), but other genes may not, having simply evolved imprinting to follow the lead of their interacting partners.

show abstract

Epistasis as a Source of Increased Additive Genetic Variance at Population Bottlenecks

Cited by 142 publications

References 0 publications

The effect of gene interactions on the long-term response to selection

The effect of gene interactions on the long-term response to selection

Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana

Evolution of genomic imprinting as a coordinator of coadapted gene expression

Contact Info

Product

Resources

About