Evolution as fitness landscape navigation: Concepts, Measures, and Emerging Questions

TL;DR

This review synthesizes recent advances in understanding how populations navigate rugged fitness landscapes, emphasizing concepts, measures, and emerging questions in evolutionary landscape research.

Contribution

It introduces a new measure of navigability based on evolutionary outcomes and clarifies key concepts and relationships in fitness landscape studies.

Findings

Relationships between epistasis, ruggedness, and navigability are complex and sometimes counterintuitive.

Large neutral networks influence evolutionary dynamics on fitness landscapes.

A new broadly applicable measure of landscape navigability is proposed.

Abstract

Fitness landscapes are mappings between genotypes, phenotypes, and fitness that shape evolution. In recent years, empirical work and theoretical models have greatly advanced our understanding of how populations navigate rugged fitness landscapes. Here, we provide a timely review of this field. Its rapidly growing literature employs a wide range of terms, which are sometimes used ambiguously or inconsistently. We therefore begin by defining the major concepts and the field's vocabulary, highlighting our own terminology choices wherever needed. We then review key results on the relationships between epistasis, ruggedness, accessibility, and navigability for genotype-fitness maps, highlighting several complex and sometimes counterintuitive connections that have emerged. Further, we review how the conserved structural properties of the underlying genotype-phenotype map -- that leads to the formation of large connected neutral networks of genotypes -- influence dynamics on fitness landscapes. We then compare the two levels to study landscape navigation -- the level of the genotype-phenotype maps and the level of genotype-fitness maps. Our review leads us to propose a new measure of navigability, based on evolutionary outcomes, that is broadly applicable and overcomes limitations of existing measures. Finally, we review the smaller body of work that relaxes the common assumption of fitness-monotonic paths on static landscapes, and discuss how this can fundamentally change the nature of fitness landscape navigation. Throughout the review, we identify directions for future work to fill existing gaps and to synthesize the disparate strands of research within the field.