Adaptive multiscapes: an up-to-date metaphor to visualize molecular adaptation

Abstract

BackgroundWright’s metaphor of the fitness landscape has shaped and conditioned our view of the adaptation of populations for almost a century. Since its inception, and including criticism raised by Wright himself, the concept has been surrounded by controversy. Among others, the debate stems from the intrinsic difficulty to capture important features of the space of genotypes, such as its high dimensionality or the existence of abundant ridges, in a visually appealing two-dimensional picture. Two additional currently widespread observations come to further constrain the applicability of the original metaphor: the very skewed distribution of phenotype sizes (which may actively prevent, due to entropic effects, the achievement of fitness maxima), and functional promiscuity (i.e. the existence of secondary functions which entail partial adaptation to environments never encountered before by the population).ResultsHere we revise some of the shortcomings of the fitness landscape metaphor and propose a new “scape” formed by interconnected layers, each layer containing the phenotypes viable in a given environment. Different phenotypes within a layer are accessible through mutations with selective value, while neutral mutations cause displacements of populations within a phenotype. A different environment is represented as a separated layer, where phenotypes may have new fitness values, other phenotypes may be viable, and the same genotype may yield a different phenotype, representing genotypic promiscuity. This scenario explicitly includes the many-to-many structure of the genotype-to-phenotype map. A number of empirical observations regarding the adaptation of populations in the light of adaptive multiscapes are reviewed.ConclusionsSeveral shortcomings of Wright’s visualization of fitness landscapes can be overcome through adaptive multiscapes. Relevant aspects of population adaptation, such as neutral drift, functional promiscuity or environment-dependent fitness, as well as entropic trapping and the concomitant impossibility to reach fitness peaks are visualized at once. Adaptive multiscapes should aid in the qualitative understanding of the multiple pathways involved in evolutionary dynamics.ReviewersThis article was reviewed by Eugene Koonin and Ricard Solé.

Differences in adaptive dynamics determine the success of virus variants that propagate together

“…Adaptation usually occurs at a local scale, by fixing one or a few mutations that confer an immediate advantage to populations. The typical time subsequently spent in this metastable state (a local fitness maximum) can be so large that, in all likelihood, the global maximum is never observed, and this local maximum works in practice as the asymptotic mutation-selection equilibrium ( Catalán et al. 2017 ).…”

On the networked architecture of genotype spaces and its critical effects on molecular evolution

“…In the dynamical framework of competition between networks, each phenotype represents now a distinguishable network characterized by its size, connectivity and fitness level. Connector links correspond to regions of apposition between the two networks, which exist in most cases (in particular when the two phenotypes considered are common) but are difficult to find if populations are finite due to the vastness of genotype spaces and NN [ 30 ]. Also, the connector links might join regions with similar fitness but different internal connectivity, or regions with different fitness, among many other possibilities.…”

“…This latter case seems to be much more common than previously thought, meaning that the co-option of promiscuous, secondary gene functions [ 29 ] is likely a common adaptive mechanism. From a formal viewpoint, therefore, the complexity of the GP map implies that fitness landscapes should be visualized as high-dimensional and interwoven sets of networks that unfold into multiple layers under environmental change [ 30 ]. New techniques, in particular the use of deep sequencing and powerful massive ways to evaluate the fitness of individual genotypes, represent a breakthrough in the empirical characterization of the complex genotype-to-phenotype-to-function relationship [ 31 , 32 ].…”

“…The architecture of genotype spaces and the dynamics of evolving molecular populations are two sides of the same coin. 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 ].…”

Phase Transitions in Virology

“…Indeed, it has been recently suggested that the dominant view among biologists of a static fitness landscape as a succession of valleys and peaks may be misleading to explain many ob-servations in virus evolution. Instead, it has been suggested that an adaptive multiscape (Catalán et al 2017), or a time-fluctuating adaptive seascape (Mustonen and Lässig 2009), may provide a much better representation.…”