Mutational robustness quantifies the effect of random mutations on fitness. When mutational robustness is high, most mutations do not change fitness or have only a minor effect on it. From the point of view of fitness landscapes, robust genotypes form neutral networks of almost equal fitness. Using deterministic population models it has been shown that selection favors genotypes inside such networks, which results in increased mutational robustness. Here we demonstrate that this effect is massively enhanced by recombination. Our results are based on a detailed analysis of mesa-shaped fitness landscapes, where we derive precise expressions for the dependence of the robustness on the landscape parameters for recombining and non-recombining populations. In addition, we carry out numerical simulations on different types of random holey landscapes as well as on an empirical fitness landscape. We show that the mutational robustness of a genotype generally correlates with its recombination weight, a new measure that quantifies the likelihood for the genotype to arise from recombination. We argue that the favorable effect of recombination on mutational robustness is a highly universal feature that may have played an important role in the emergence and maintenance of mechanisms of genetic exchange.
Understanding the benefits and costs of recombination under different scenarios of evolutionary adaptation remains an open problem for theoretical and experimental research. In this study, we focus on finite populations evolving on neutral networks comprising viable and unfit genotypes. We provide a comprehensive overview of the effects of recombination by jointly considering different measures of evolvability and mutational robustness over a broad parameter range, such that many evolutionary regimes are covered. We find that several of these measures vary non-monotonically with the rates of mutation and recombination. Moreover, the presence of unfit genotypes that introduce inhomogeneities in the network of viable states qualitatively alters the effects of recombination. We conclude that conflicting trends induced by recombination can be explained by an emerging trade-off between evolvability on the one hand, and mutational robustness on the other. Finally, we discuss how different implementations of the recombination scheme in theoretical models can affect the observed dependence on recombination rate through a coupling between recombination and genetic drift.
Many effects attributed to recombination have been invoked to explain the advantage of sex. The most prominent arguments focus on either evolvability, genetic diversity, or mutational robustness to justify why the benefit of recombination overcomes its costs, with partially contradicting results. As a consequence, understanding which aspects of recombination are most important in a given situation remains an open problem for theoretical and experimental research. In this study, we focus on finite populations evolving on neutral networks, which already display remarkably complex behavior. We aim to provide a comprehensive overview of the effects of recombination by jointly considering different measures of evolvability, genetic diversity, and mutational robustness over a broad parameter range, such that many evolutionary regimes are covered. We find that several of these measures vary non-monotonically with the rates of mutation and recombination. Moreover, the presence of lethal genotypes that introduce inhomogeneities in the network of viable states qualitatively alters the effects of recombination. We conclude that conflicting trends induced by recombination can be explained by an emerging trade-off between evolvability and genetic diversity on the one hand, and mutational robustness and fitness on the other. Finally, we discuss how different implementations of the recombination scheme in theoretical models can affect the observed dependence on recombination rate through a coupling between recombination and genetic drift.
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