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Evolutionary Accessibility in Tunably Rugged Fitness Landscapes

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Abstract

The adaptive evolution of a population under the influence of mutation and selection is strongly influenced by the structure of the underlying fitness landscape, which encodes the interactions between mutations at different genetic loci. Theoretical studies of such landscapes have been carried out for several decades, but only recently experimental fitness measurements encompassing all possible combinations of small sets of mutations have become available. The empirical studies have spawned new questions about the accessibility of optimal genotypes under natural selection. Depending on population dynamic parameters such as mutation rate and population size, evolutionary accessibility can be quantified through the statistics of accessible mutational pathways (along which fitness increases monotonically), or through the study of the basin of attraction of the optimal genotype under greedy (steepest ascent) dynamics. Here we investigate these two measures of accessibility in the framework of Kauffman’s LK-model, a paradigmatic family of random fitness landscapes with tunable ruggedness. The key parameter governing the strength of genetic interactions is the number K of interaction partners of each of the L sites in the genotype sequence. In general, accessibility increases with increasing genotype dimensionality L and decreases with increasing number of interactions K. Remarkably, however, we find that some measures of accessibility behave non-monotonically as a function of K, indicating a special role of the most sparsely connected, non-trivial cases K=1 and 2. The relation between models for fitness landscapes and spin glasses is also addressed.

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Notes

  1. In the terminology of stochastic processes, this is the ‘diffusive’ term in the Fokker-Planck equation describing the probability distribution of mutant frequencies, while the term describing the deterministic behavior is usually called ‘drift’. Since in almost all that follows, only selection will be considered, this should not lead to confusion.

  2. For an empirical analysis of accessible pathways that includes the possibility of mutational reversions see [27].

  3. At least for the HoC and RMF models described below, it can be shown that the statistics of accessible paths to the global maximum does not depend on the choice of the starting point.

  4. The factor λ=1 or 2 depending on the population dynamic model, see [36].

  5. The model is generally known as the ‘NK model’. Here we follow the convention of most population genetic literature in reserving the letter N for population size and designating the number of loci by L.

  6. Often the sum on the right hand side of (3) is scaled by L −1 or L −1/2 in order to guarantee the existence of the limit L→∞. Here only the rank ordering of fitness is of interest and the overall magnitude of F is irrelevant.

  7. Note that, in contrast to the peaks seen in Fig. 4, the gap does not live on the scale L!, since Δn/L!→0 for L→∞.

  8. Note that this estimate relies on uniformly sampling all local maxima. The size of a typical basin found by a greedy walk starting at a random position will be larger, because this introduces a bias towards larger basins.

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Acknowledgements

We would like to thank Johannes Berg, Anton Bovier, Bernard Derrida and Remi Monasson for useful discussions and remarks, and Alexander Klözer for his contributions in the initial stages of this project. This work was supported by DFG within SFB 680 and BCGS. JF acknowledges financial support from Studienstiftung des deutschen Volkes.

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Franke, J., Krug, J. Evolutionary Accessibility in Tunably Rugged Fitness Landscapes. J Stat Phys 148, 706–723 (2012). https://doi.org/10.1007/s10955-012-0507-9

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