Ecology shapes epistasis in a genotype–phenotype–fitness map for stick insect colour

Genetic interactions such as epistasis are widespread in nature and can shape evolutionary dynamics. Epistasis occurs due to nonlinearity in biological systems, which can arise via cellular processes that convert genotype to phenotype and via selective processes that connect phenotype to fitness. Few studies in nature have connected genotype to phenotype to fitness for multiple potentially interacting genetic variants. Thus, the causes of epistasis in the wild remain poorly understood. Here, we show that epistasis for fitness is an emergent and predictable property of nonlinear selective processes. We do so by measuring the genetic basis of cryptic colouration and survival in a field experiment with stick insects. We find that colouration shows a largely additive genetic basis but with some effects of epistasis that enhance differentiation between colour morphs. In terms of fitness, different combinations of loci affecting colouration confer high survival in one host-plant treatment. Specifically, nonlinear correlational selection for specific combinations of colour traits in this treatment drives the emergence of pairwise and higher-order epistasis for fitness at loci underlying colour. In turn, this results in a rugged fitness landscape for genotypes. In contrast, fitness epistasis was dampened in another treatment, where selection was weaker. Patterns of epistasis that are shaped by ecologically based selection could be common and central to understanding fitness landscapes, the dynamics of evolution and potentially other complex systems.