The variability of evolvability: properties of dynamic fitness landscapes determine how phenotypic variability evolves

Abstract The magnitude and shape of phenotypic variation depends on properties of the genotype-to-phenotype (GP) map, which itself can evolve over time. The evolution of GP maps is particularly interesting in variable environments, as GP maps can evolve to bias variation in the direction of past selection, increasing the evolvability of the population over time. However, the degree and manner in which environmental variation shapes GP maps and influences evolutionary dynamics may depend on properties of the fitness landscape. To explore how evolutionary dynamics are affected by variable environments across a wide range of different pairs of fitness landscapes, we evolved GP maps to produce spatial-temporal gene expression patterns that matched two-dimensional patterns generated by different elementary cellular automata (CA) rules. We found remarkable variation in how populations evolved in variable environments. In some cases, changing the environment helped populations find higher fitness peaks; in others, it hindered them. The evolution of evolvability also depended on the fitness landscape pair. In some experiments, the ability to generate adaptive phenotypic variation upon environment change increased over time, while in some others, populations found shared areas between fitness landscapes. On the other hand, environmental variability consistently resulted in higher fitness landscape exploration, average fitness and mutational robustness compared to evolution in static environments, which we hypothesize are tightly connected. In conclusion, work presented here sheds light on important general consequences of environmental variability, while also demonstrating dependency on properties of fitness landscapes, which future research on the evolution of evolvability should consider. Significance statement The speed and direction of evolution depend on the availability of phenotypic variation. Genotype-to-phenotype maps can over time bias phenotypic variability to more readily produce alternative adaptive phenotypes in fluctuating environments. However, because properties of the fitness landscapes influence evolutionary dynamics, it remains unclear which previously observed dynamics reflect general effects of environmental variability and which are specific to the pair of landscapes used. We found that the height of the fitness peaks discovered, and how the populations became more evolvable, significantly differed across landscape pairs. In contrast, environmental variability consistently increased average fitness and mutational robustness. Thus, future research investigating the inherent consequences of frequent environmental change should be done on a range of dynamic landscapes. Competing Interest Statement The authors have declared no competing interest. Footnotes Minor fixes of citations and funding information.