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Gene duplication and subsequent diversification strongly affect phenotypic evolvability and robustness.

ABSTRACT: We study the effects of non-determinism and gene duplication on the structure of genotype-phenotype (GP) maps by introducing a non-deterministic version of the Polyomino self-assembly model. This model has previously been used in a variety of contexts to model the assembly and evolution of protein quaternary structure. Firstly, we show the limit of the current deterministic paradigm which leads to built-in anti-correlation between evolvability and robustness at the genotypic level. We develop a set of metrics to measure structural properties of GP maps in a non-deterministic setting and use them to evaluate the effects of gene duplication and subsequent diversification. Our generalized versions of evolvability and robustness exhibit positive correlation for a subset of genotypes. This positive correlation is only possible because non-deterministic phenotypes can contribute to both robustness and evolvability. Secondly, we show that duplication increases robustness and reduces evolvability initially, but that the subsequent diversification that duplication enables has a stronger, inverse effect, greatly increasing evolvability and reducing robustness relative to their original values.

SUBMITTER: Jouffrey V

PROVIDER: S-EPMC8220273 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Gene duplication and subsequent diversification strongly affect phenotypic evolvability and robustness.

Jouffrey V V Leonard A S AS Ahnert S E SE

Royal Society open science 20210623 6

We study the effects of non-determinism and gene duplication on the structure of genotype-phenotype (GP) maps by introducing a non-deterministic version of the Polyomino self-assembly model. This model has previously been used in a variety of contexts to model the assembly and evolution of protein quaternary structure. Firstly, we show the limit of the current deterministic paradigm which leads to built-in anti-correlation between evolvability and robustness at the genotypic level. We develop a ...[more]

PMID: 34168886

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Project description:BackgroundResearch on gene duplication is abundant and comes from a wide range of approaches, from high-throughput analyses and experimental evolution to bioinformatics and theoretical models. Notwithstanding, a consensus is still lacking regarding evolutionary mechanisms involved in evolution through gene duplication as well as the conditions that affect them. We argue that a better understanding of evolution through gene duplication requires considering explicitly that genes do not act in isolation. It demands studying how the perturbation that gene duplication implies percolates through the web of gene interactions. Due to evolution's contingent nature, the paths that lead to the final fate of duplicates must depend strongly on the early stages of gene duplication, before gene copies have accumulated distinctive changes.MethodsHere we use a widely-known model of gene regulatory networks to study how gene duplication affects network behavior in early stages. Such networks comprise sets of genes that cross-regulate. They organize gene activity creating the gene expression patterns that give cells their phenotypic properties. We focus on how duplication affects two evolutionarily relevant properties of gene regulatory networks: mitigation of the effect of new mutations and access to new phenotypic variants through mutation.ResultsAmong other observations, we find that those networks that are better at maintaining the original phenotype after duplication are usually also better at buffering the effect of single interaction mutations and that duplication tends to enhance further this ability. Moreover, the effect of mutations after duplication depends on both the kind of mutation and genes involved in it. We also found that those phenotypes that had easier access through mutation before duplication had higher chances of remaining accessible through new mutations after duplication.ConclusionOur results support that gene duplication often mitigates the impact of new mutations and that this effect is not merely due to changes in the number of genes. The work that we put forward helps to identify conditions under which gene duplication may enhance evolvability and robustness to mutations.

Project description:Cellular phenotypes underpinned by regulatory networks need to respond to evolutionary pressures to allow adaptation, but at the same time be robust to perturbations. This creates a conflict in which mutations affecting regulatory networks must both generate variance but also be tolerated at the phenotype level. Here, we perform mathematical analyses and simulations of regulatory networks to better understand the potential trade-off between robustness and evolvability. Examining the phenotypic effects of mutations, we find an inverse correlation between robustness and evolvability that breaks only with nonlinearity in the network dynamics, through the creation of regions presenting sudden changes in phenotype with small changes in genotype. For genotypes embedding low levels of nonlinearity, robustness and evolvability correlate negatively and almost perfectly. By contrast, genotypes embedding nonlinear dynamics allow expression levels to be robust to small perturbations, while generating high diversity (evolvability) under larger perturbations. Thus, nonlinearity breaks the robustness-evolvability trade-off in gene expression levels by allowing disparate responses to different mutations. Using analytical derivations of robustness and system sensitivity, we show that these findings extend to a large class of gene regulatory network architectures and also hold for experimentally observed parameter regimes. Further, the effect of nonlinearity on the robustness-evolvability trade-off is ensured as long as key parameters of the system display specific relations irrespective of their absolute values. We find that within this parameter regime genotypes display low and noisy expression levels. Examining the phenotypic effects of mutations, we find an inverse correlation between robustness and evolvability that breaks only with nonlinearity in the network dynamics. Our results provide a possible solution to the robustness-evolvability trade-off, suggest an explanation for the ubiquity of nonlinear dynamics in gene expression networks, and generate useful guidelines for the design of synthetic gene circuits.

Dataset Information

Gene duplication and subsequent diversification strongly affect phenotypic evolvability and robustness.

Publications

Gene duplication and subsequent diversification strongly affect phenotypic evolvability and robustness.

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