Evolvability Costs of Niche Expansion

What prevents generalists from displacing specialists, despite obvious competitive advantages of utilizing a broad niche? The classic genetic explanation is antagonistic pleiotropy: genes underlying the generalism produce ‘jacks-of-all-trades’ that are masters of none. However, experiments challenge this assumption that mutations enabling niche expansion must reduce fitness in other environments. Theory suggests an alternative cost of generalism: decreased evolvability, or the reduced capacity to adapt. Generalists using multiple environments experience relaxed selection in any one environment, producing greater relative lag load. Additionally, mutations fixed by generalist lineages early during their evolution that avoid or compensate for antagonistic pleiotropy may limit access to certain future evolutionary trajectories. Hypothesized evolvability costs of generalism warrant further exploration, and we suggest outstanding questions meriting attention. Given the obvious benefit from utilizing diverse resources, what prevents populations and communities from being dominated by generalists? Classical explanations hold that a ‘jack-of-all-trades’ is a master of none, meaning that niche-expanding mutations decrease fitness in the original environment (antagonistic pleiotropy).We suggest an alternative cost to generalism: reduced evolvability. Generalists experience selection in multiple environments, relaxing the effects in any one environment, and forcing adaptive mutations through multiple environmental filters or compensatory mutations. These factors lead to generalists experiencing lag load, conceptualized as a more rugged fitness landscape.Although this hypothesis has not been tested explicitly, we provide evidence for the elements of it from models of eco-evolutionary dynamics and experimental evolution.