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Abstract:

Engineers routinely design systems to be modular and symmetric in order to increase robustness to perturbations and to facilitate alterations at a later date. Biological structures also frequently exhibit modularity and symmetry, but the origin of such trends is much less well understood. It can be tempting to assume – by analogy to engineering design – that symmetry and modularity arise from natural selection. But evolution, unlike engineers, cannot plan ahead, and so these traits must also afford some immediate selective advantage which is hard to reconcile with the breadth of systems where symmetry is observed. Here we introduce an alternative non-adaptive hypothesis based on an algorithmic picture of evolution. It suggests that symmetric structures preferentially arise not just due to natural selection, but also because they require less specific information to encode, and are therefore much more likely to appear as phenotypic variation through random mutations. Arguments from algorithmic information theory can formalise this intuition, leading to the prediction that many genotype-phenotype maps are exponentially biased towards phenotypes with low descriptional complexity. A preference for symmetry is a special case of this bias towards compressible descriptions. We test these predictions with extensive biological data, showing that that protein complexes, RNA secondary structures, and a model gene-regulatory network all exhibit the expected exponential bias towards simpler (and more symmetric) phenotypes. Lower descriptional complexity also correlates with higher mutational robustness, which may aid the evolution of complex modular assemblies of multiple components.

Abstract:

Counterfactual questions such as "what would happen if you re-run the tape of life?" turn on the nature of the landscape of biological possibilities. Since the number of potential sequences that store genetic information grows exponentially with length, genetic possibility spaces can be so unimaginably vast that commentators frequently reach of hyper-astronomical metaphors that compare their size to that of the universe. Re-run the tape of life and the likelihood of encountering the same sequences in such hyper-astronomically large spaces is infinitesimally small, suggesting that evolutionary outcomes are highly contingent. On the other hand, the wide-spread occurrence of evolutionary convergence implies that similar phenotypes can be found again with relative ease. How can this be? Part of the solution to this conundrum must lie in the manner that genotypes map to phenotypes. By studying simple genotype-phenotype maps, where the counterfactual space of all possible phenotypes can be enumerated, it is shown that strong bias in the arrival of variation may explain why certain phenotypes are (repeatedly) observed in nature, while others never appear. This biased variation provides a non-selective cause for certain types of convergence. It illustrates how the role of randomness and contingency may differ significantly between genetic and phenotype spaces.

Abstract:

Abstract Ruggedness — the prevalence of fitness peaks — and navigability — the existence of fitness-increasing paths to a target — are key factors affecting evolution on fitness landscapes. Here, we analyse these properties in landscapes that inherit biophysically grounded genotype–phenotype (GP) maps. By assuming a random phenotype-fitness assignment as a baseline, the structure of the GP maps is included without imposing further fitness correlations. We show analytically that the expected ruggedness can be predicted from two quantities: the sizes of neutral components (NCs)—mutationally connected genotype sets with the same phenotype—and their evolvabilities, defined as the number of distinct phenotypes among the NC's mutational neighbours. Other features —such as robustness— influence ruggedness only indirectly via correlations with evolvability. Numerical results across diverse GP maps confirm that NC size and evolvability alone suffice to predict both the mean prevalence and heights of peaks. These calculations also provide new insights: Under random phenotype-fitness assignment, peaks arising from high-evolvability NCs have higher expected fitness than those from low-evolvability NCs. Thus, when evolvability correlates positively with NC size, the formation of large low-fitness peaks is impeded. We further derive an approximate scaling law for the minimal average evolvability required for navigability. Our framework applies broadly across GP maps, providing general insight into when and why fitness landscapes are expected to be rugged or navigable.