Effects of Recombination on Complex Regulatory Circuits

Martin, O. C.; Wagner, Andreas

doi:10.1534/genetics.109.104174

Cited by 53 publications

(80 citation statements)

References 55 publications

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“…We documented two differences between sexual and asexual populations that likely affected the evolution of U d : First, sexual populations uniquely experienced recombination load, L R : We know from previous work that selection to minimize L R ; alone, results in increasing robustness to both recombination and mutation, lowering U d (Azevedo et al 2006;Gardner and Kalinka 2006;Misevic et al 2006;Martin and Wagner 2009;Lohaus et al 2010). Second, asexual populations uniquely experienced Hill-Robertson interference that reduced N e ( Figure 3B).…”

Section: Discussionmentioning

confidence: 87%

“…We found that Hill-Robertson interference also played a role in our model in creating both a longterm and a short-term advantage of sex. But we also showed that the long-and short-term advantages of sex were determined by differences between sexual and asexual populations in the evolutionary dynamics of two properties of the genetic architecture, U d and L R : We next sought to quantify the contribution of Hill-Robertson interference to these dynamics.We documented two differences between sexual and asexual populations that likely affected the evolution of U d : First, sexual populations uniquely experienced recombination load, L R : We know from previous work that selection to minimize L R ; alone, results in increasing robustness to both recombination and mutation, lowering U d (Azevedo et al 2006;Gardner and Kalinka 2006;Misevic et al 2006;Martin and Wagner 2009;Lohaus et al 2010). Second, asexual populations uniquely experienced Hill-Robertson interference that reduced N e ( Figure 3B).…”

mentioning

confidence: 87%

“…First, the greater number of genes allows mutations to have a broad range of potential fitness effects, including beneficial, neutral, slightly deleterious, and lethal. Second, the higher U allows populations to show considerable mutation load at equilibrium (see Box 1) (Martin and Wagner 2009). Third, real gene networks are relatively sparse (Leclerc 2008).…”

Section: Parameter Valuesmentioning

confidence: 99%

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An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

et al. 2016

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Sex is ubiquitous in the natural world, but the nature of its benefits remains controversial. Previous studies have suggested that a major advantage of sex is its ability to eliminate interference between selection on linked mutations, a phenomenon known as HillRobertson interference. However, those studies may have missed both important advantages and important disadvantages of sexual reproduction because they did not allow the distributions of mutational effects and interactions (i.e., the genetic architecture) to evolve. Here we investigate how Hill-Robertson interference interacts with an evolving genetic architecture to affect the evolutionary origin and maintenance of sex by simulating evolution in populations of artificial gene networks. We observed a long-term advantage of sexequilibrium mean fitness of sexual populations exceeded that of asexual populations-that did not depend on population size. We also observed a short-term advantage of sex-sexual modifier mutations readily invaded asexual populations-that increased with population size, as was observed in previous studies. We show that the long-and short-term advantages of sex were both determined by differences between sexual and asexual populations in the evolutionary dynamics of two properties of the genetic architecture: the deleterious mutation rate (U d ) and recombination load (L R ). These differences resulted from a combination of selection to minimize L R ; which is experienced only by sexuals, and Hill-Robertson interference experienced primarily by asexuals. In contrast to the previous studies, in which Hill-Robertson interference had only a direct impact on the fitness advantages of sex, the impact of Hill-Robertson interference in our simulations was mediated additionally by an indirect impact on the efficiency with which selection acted to reduce U d : KEYWORDS evolution of sex; gene network; deleterious mutation rate; recombination load; population size T HE vast majority of organisms alive today have experienced some form of genetic exchange, or sex, in their recent evolutionary history, despite substantial costs (Weismann 1887;Maynard Smith 1978;Bell 1982;Otto and Lenormand 2002). Sex breaks up favorable genetic combinations and increases the risk of transmission of pathogens and selfish genetic elements. Sexual reproduction is often slower than asexual reproduction. In many sexually reproducing eukaryotes, sex involves costs of finding and attracting a mate and of mating in itself; in anisogamous species, if one sex contributes little to progeny production, sexual reproduction carries a twofold cost of producing that sex. The ubiquity of sex implies that it must confer considerable benefits to overcome these costs. However, the nature of these benefits is not well understood. In fact, .20 hypotheses have been proposed to explain the benefits of sex (Bell 1982;Kondrashov 1993;Hurst and Peck 1996;Otto and Lenormand 2002). While hypotheses predicting direct benefits exist [e.g., improved DNA repair (Bernstein et al. 1985)], t...

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Section: Discussionmentioning

confidence: 87%

mentioning

confidence: 87%

Section: Parameter Valuesmentioning

confidence: 99%

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An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

et al. 2016

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“…Interestingly, this response might promote the maintenance of recombination through the more efficient elimination of deleterious mutations [20]. It was also found that circuits evolved with recombination were enriched for cis-regulatory complexes [12], and hence had an increased modular structure. Evolution experiments with digital organisms similarly found that recombination increased robustness and modularity, and reduced unidimensional epistasis [13].…”

Section: (D) Robustnessmentioning

confidence: 99%

The causes of epistasis

2011

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Since Bateson's discovery that genes can suppress the phenotypic effects of other genes, gene interactions-called epistasis-have been the topic of a vast research effort. Systems and developmental biologists study epistasis to understand the genotype -phenotype map, whereas evolutionary biologists recognize the fundamental importance of epistasis for evolution. Depending on its form, epistasis may lead to divergence and speciation, provide evolutionary benefits to sex and affect the robustness and evolvability of organisms. That epistasis can itself be shaped by evolution has only recently been realized. Here, we review the empirical pattern of epistasis, and some of the factors that may affect the form and extent of epistasis. Based on their divergent consequences, we distinguish between interactions with or without mean effect, and those affecting the magnitude of fitness effects or their sign. Empirical work has begun to quantify epistasis in multiple dimensions in the context of metabolic and fitness landscape models. We discuss possible proximate causes (such as protein function and metabolic networks) and ultimate factors (including mutation, recombination, and the importance of natural selection and genetic drift). We conclude that, in general, pleiotropy is an important prerequisite for epistasis, and that epistasis may evolve as an adaptive or intrinsic consequence of changes in genetic robustness and evolvability.

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“…In addition to extensive studies on mutational robustness and evolvability, it has been proposed recently in the context of gene regulatory circuits that recombination can create novel phenotypes more efficiently with a much less disruptive effect than mutation [20,33]. It is argued that recombination reorganizes genes and gene circuits and thus has greater phenotypic consequences than point mutation.…”

Section: Introductionmentioning

confidence: 99%

Robustness and Evolvability of Recombination in Linear Genetic Programming

Banzhaf

Moore

2013

Lecture Notes in Computer Science

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Abstract. The effect of neutrality on evolutionary search is known to be crucially dependent on the distribution of genotypes over phenotypes. Quantitatively characterizing robustness and evolvability in genotype and phenotype spaces greatly helps to understand the influence of neutrality on Genetic Programming. Most existing robustness and evolvability studies focus on mutations with a lack of investigation of recombinational operations. Here, we extend a previously proposed quantitative approach of measuring mutational robustness and evolvability in Linear GP. By considering a simple LGP system that has a compact representation and enumerable genotype and phenotype spaces, we quantitatively characterize the robustness and evolvability of recombination at the phenotypic level. In this simple yet representative LGP system, we show that recombinational properties are correlated with mutational properties. Utilizing a population evolution experiment, we demonstrate that recombination significantly accelerates the evolutionary search process and particularly promotes robust phenotypes that innovative phenotypic explorations.

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Effects of Recombination on Complex Regulatory Circuits

Cited by 53 publications

References 55 publications

An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

The causes of epistasis

Robustness and Evolvability of Recombination in Linear Genetic Programming

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