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Effects of ploidy and recombination on evolution of robustness in a model of the segment polarity network.

Kim KJ, Fernandes VM - PLoS Comput. Biol. (2009)

Bottom Line: Robustness was measured by simulating a mutation in the network and measuring the effect on the engrailed and wingless patterns; higher robustness corresponded to insensitivity of this pattern to perturbation.We compared robustness in diploid and haploid populations, with either asexual or sexual reproduction.In all cases, robustness increased, and the greatest increase was in diploid sexual populations; diploidy and sex synergized to evolve greater robustness than either acting alone.

View Article: PubMed Central - PubMed

Affiliation: Center for Cell Dynamics, Friday Harbor Labs, University of Washington, Friday Harbor, Washington, USA. kjkim@u.washington.edu

ABSTRACT
Many genetic networks are astonishingly robust to quantitative variation, allowing these networks to continue functioning in the face of mutation and environmental perturbation. However, the evolution of such robustness remains poorly understood for real genetic networks. Here we explore whether and how ploidy and recombination affect the evolution of robustness in a detailed computational model of the segment polarity network. We introduce a novel computational method that predicts the quantitative values of biochemical parameters from bit sequences representing genotype, allowing our model to bridge genotype to phenotype. Using this, we simulate 2,000 generations of evolution in a population of individuals under stabilizing and truncation selection, selecting for individuals that could sharpen the initial pattern of engrailed and wingless expression. Robustness was measured by simulating a mutation in the network and measuring the effect on the engrailed and wingless patterns; higher robustness corresponded to insensitivity of this pattern to perturbation. We compared robustness in diploid and haploid populations, with either asexual or sexual reproduction. In all cases, robustness increased, and the greatest increase was in diploid sexual populations; diploidy and sex synergized to evolve greater robustness than either acting alone. Diploidy conferred increased robustness by allowing most deleterious mutations to be rescued by a working allele. Sex (recombination) conferred a robustness advantage through "survival of the compatible": those alleles that can work with a wide variety of genetically diverse partners persist, and this selects for robust alleles.

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Related in: MedlinePlus

Distinguishing effects of mutation from recombination.(A) Fraction of mutated individuals that were viable during evolutionarysimulation. (B) Fraction of dead individuals during the simulation thatdid not have a mutation. A dramatically higher fraction of deaths werecaused by recombination in sexual diploid populations than sexualhaploid. (C) Fitness load calculated from Equation 16. Plots showaverage of 40 simulations, smoothed with a sliding window over 50generations.
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pcbi-1000296-g006: Distinguishing effects of mutation from recombination.(A) Fraction of mutated individuals that were viable during evolutionarysimulation. (B) Fraction of dead individuals during the simulation thatdid not have a mutation. A dramatically higher fraction of deaths werecaused by recombination in sexual diploid populations than sexualhaploid. (C) Fitness load calculated from Equation 16. Plots showaverage of 40 simulations, smoothed with a sliding window over 50generations.

Mentions: Why does sex produce more robust populations? In our simulations, individualshave reduced fitness/survivorship if they fail to sharpen the correct en and wgpatterns sufficiently. Fitness/survivorship can be reduced by two sources: a newmutation or, in sexual populations, recombination of alleles that do notfunction properly together. Figure6 shows the relative effect of recombination and mutation onsurvival. During the simulation, we recorded the number of dead individuals andtheir genotypes, and whether they had a new mutation. Figure 6A shows the fraction of individualswith a new mutation that were viable. This data is qualitatively consistent withFigure 5A, but includesmutations that could alter multiple genes and bit-sequences during evolution. Todetermine how often recombination produced incompatible allele combinations, wemeasured the fraction of deaths where individuals did not have a new mutation(i.e. the fraction of the dead due to recombination). Figure 6B shows diploid sexual populationsshowed a near doubling of this fraction compared to the haploid sexualpopulations. Thus, diploid sexual populations experience a greater pressure tomaintain alleles that both produce the correct phenotype and that are alsohighly compatible with the other alleles in the population. Recombinationconstantly produces new allele combinations that cause quantitative variation;thus sexual populations (especially diploid sexual populations) more stronglyselect for genotypes (and alleles) that are robust to quantitative variation.


Effects of ploidy and recombination on evolution of robustness in a model of the segment polarity network.

Kim KJ, Fernandes VM - PLoS Comput. Biol. (2009)

Distinguishing effects of mutation from recombination.(A) Fraction of mutated individuals that were viable during evolutionarysimulation. (B) Fraction of dead individuals during the simulation thatdid not have a mutation. A dramatically higher fraction of deaths werecaused by recombination in sexual diploid populations than sexualhaploid. (C) Fitness load calculated from Equation 16. Plots showaverage of 40 simulations, smoothed with a sliding window over 50generations.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2637435&req=5

pcbi-1000296-g006: Distinguishing effects of mutation from recombination.(A) Fraction of mutated individuals that were viable during evolutionarysimulation. (B) Fraction of dead individuals during the simulation thatdid not have a mutation. A dramatically higher fraction of deaths werecaused by recombination in sexual diploid populations than sexualhaploid. (C) Fitness load calculated from Equation 16. Plots showaverage of 40 simulations, smoothed with a sliding window over 50generations.
Mentions: Why does sex produce more robust populations? In our simulations, individualshave reduced fitness/survivorship if they fail to sharpen the correct en and wgpatterns sufficiently. Fitness/survivorship can be reduced by two sources: a newmutation or, in sexual populations, recombination of alleles that do notfunction properly together. Figure6 shows the relative effect of recombination and mutation onsurvival. During the simulation, we recorded the number of dead individuals andtheir genotypes, and whether they had a new mutation. Figure 6A shows the fraction of individualswith a new mutation that were viable. This data is qualitatively consistent withFigure 5A, but includesmutations that could alter multiple genes and bit-sequences during evolution. Todetermine how often recombination produced incompatible allele combinations, wemeasured the fraction of deaths where individuals did not have a new mutation(i.e. the fraction of the dead due to recombination). Figure 6B shows diploid sexual populationsshowed a near doubling of this fraction compared to the haploid sexualpopulations. Thus, diploid sexual populations experience a greater pressure tomaintain alleles that both produce the correct phenotype and that are alsohighly compatible with the other alleles in the population. Recombinationconstantly produces new allele combinations that cause quantitative variation;thus sexual populations (especially diploid sexual populations) more stronglyselect for genotypes (and alleles) that are robust to quantitative variation.

Bottom Line: Robustness was measured by simulating a mutation in the network and measuring the effect on the engrailed and wingless patterns; higher robustness corresponded to insensitivity of this pattern to perturbation.We compared robustness in diploid and haploid populations, with either asexual or sexual reproduction.In all cases, robustness increased, and the greatest increase was in diploid sexual populations; diploidy and sex synergized to evolve greater robustness than either acting alone.

View Article: PubMed Central - PubMed

Affiliation: Center for Cell Dynamics, Friday Harbor Labs, University of Washington, Friday Harbor, Washington, USA. kjkim@u.washington.edu

ABSTRACT
Many genetic networks are astonishingly robust to quantitative variation, allowing these networks to continue functioning in the face of mutation and environmental perturbation. However, the evolution of such robustness remains poorly understood for real genetic networks. Here we explore whether and how ploidy and recombination affect the evolution of robustness in a detailed computational model of the segment polarity network. We introduce a novel computational method that predicts the quantitative values of biochemical parameters from bit sequences representing genotype, allowing our model to bridge genotype to phenotype. Using this, we simulate 2,000 generations of evolution in a population of individuals under stabilizing and truncation selection, selecting for individuals that could sharpen the initial pattern of engrailed and wingless expression. Robustness was measured by simulating a mutation in the network and measuring the effect on the engrailed and wingless patterns; higher robustness corresponded to insensitivity of this pattern to perturbation. We compared robustness in diploid and haploid populations, with either asexual or sexual reproduction. In all cases, robustness increased, and the greatest increase was in diploid sexual populations; diploidy and sex synergized to evolve greater robustness than either acting alone. Diploidy conferred increased robustness by allowing most deleterious mutations to be rescued by a working allele. Sex (recombination) conferred a robustness advantage through "survival of the compatible": those alleles that can work with a wide variety of genetically diverse partners persist, and this selects for robust alleles.

Show MeSH
Related in: MedlinePlus