Abstract
Evolutionary dynamics is often viewed as a subtle process of change accumulation that causes a divergence among organisms and their genomes. However, this interpretation is an inheritance of a gradualistic view that has been challenged at the macroevolutionary, ecological and molecular level. Actually, when the complex architecture of genotype spaces is taken into account, the evolutionary dynamics of molecular populations becomes intrinsically non-uniform, sharing deep qualitative and quantitative similarities with slowly driven physical systems: nonlinear responses analogous to critical transitions, sudden state changes or hysteresis, among others. Furthermore, the phenotypic plasticity inherent to genotypes transforms classical fitness landscapes into multiscapes where adaptation in response to an environmental change may be very fast. The quantitative nature of adaptive molecular processes is deeply dependent on a network-of-networks multilayered structure of the map from genotype to function that we begin to unveil.
Highlights
Gradualism posits that any profound change in nature is the result of minor cumulative modifications due to the action of slow but sustained processes
The space of genotypes can be depicted in this context by a number of interconnecting neutral networks (NNs) when each node is projected in a horizontal neutral layer whose vertical position represents its fitness value
This result cannot be extrapolated to more general fitness landscapes, where both the equilibrium state of the population and the transient dynamics depend in a non-trivial fashion on network topology and genotype fitness [103] (cf. equations (3.2) and (3.4) in box 1)
Summary
Gradualism posits that any profound change in nature is the result of minor cumulative modifications due to the action of slow but sustained processes. License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited Research in this century has unveiled a large number of cases where smooth environmental changes may trigger sudden and irreversible ecological responses [8,9]. The network-of-networks structure of genotype spaces described in realistic, though artificial, models is emerging in empirical characterizations of the diversity of molecular populations [33] Adaptive evolutionary systems, such as large-scale evolution, ecology or (molecular) populations, share deep analogies that can be likely ascribed to their networked architecture plus a non-trivial relationship between exogenous drivers and endogenous responses. The heterogeneous structure of genotype spaces and its apparently hierarchical organization as a multilayered network of networks explains, among others, punctuated dynamics [22], drift and switch transitions [24], genomic shifts [23] or Waddington’s genetic assimilation [30,34]
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