Genetic drift opposes mutualism during spatial population expansion

Significance Species expand from where they evolved or migrate in response to climate change. Such spatial expansions can impede mutualistic interactions (beneficial for both partners). Mutualism selects for species coexistence and genetic diversity, but spatial expansion creates regions of low diversity due to repeated founder effects. We show both theoretically and experimentally, using the colony expansion of cross-feeding yeast as a model system, that a critical mutualistic strength is required to “survive” spatial expansions. This constraint may have shaped the evolution of mutualisms, allowing only the spread of very beneficial mutualisms (e.g., the invasion of land by plants with mycorrhizal fungi and flowering plants with pollen-dispersing insects) or leading to additional mechanisms for coordinated partner dispersal (e.g., endosymbionts and lichens). Mutualistic interactions benefit both partners, promoting coexistence and genetic diversity. Spatial structure can promote cooperation, but spatial expansions may also make it hard for mutualistic partners to stay together, because genetic drift at the expansion front creates regions of low genetic and species diversity. To explore the antagonism between mutualism and genetic drift, we grew cross-feeding strains of the budding yeast Saccharomyces cerevisiae on agar surfaces as a model for mutualists undergoing spatial expansions. By supplying varying amounts of the exchanged nutrients, we tuned strength and symmetry of the mutualistic interaction. Strong mutualism suppresses genetic demixing during spatial expansions and thereby maintains diversity, but weak or asymmetric mutualism is overwhelmed by genetic drift even when mutualism is still beneficial, slowing growth and reducing diversity. Theoretical modeling using experimentally measured parameters predicts the size of demixed regions and how strong mutualism must be to survive a spatial expansion.