Eco-evolutionary dynamics set the tempo and trajectory of metabolic evolution in multispecies communities

The eco-evolutionary dynamics of microbial communities are predicted to affect both the tempo and trajectory of evolution in constituent species [1]. While community composition determines available niche space, species sorting dynamically alters composition, changing over time the distribution of vacant niches to which species adapt [2], altering evolutionary trajectories [3, 4]. Competition for the same niche can limit evolutionary potential if population size and mutation supply are reduced [5, 6] but, alternatively, could stimulate evolutionary divergence to exploit vacant niches if character displacement results from the coevolution of competitors [7, 8]. Under more complex ecological scenarios, species can create new niches through their exploitation of complex resources, enabling others to adapt to occupy these newly formed niches [9, 10]. Disentangling the drivers of natural selection within such communities is extremely challenging, and it is thus unclear how eco-evolutionary dynamics drive the evolution of constituent taxa. We tracked the metabolic evolution of a focal species during adaptation to wheat straw as a resource both in monoculture and in polycultures wherein on-going eco-evolutionary community dynamics were either permitted or prevented. Species interactions accelerated metabolic evolution. Eco-evolutionary dynamics drove increased use of recalcitrant substrates by the focal species, whereas greater exploitation of readily digested substrate niches created by other species evolved if on-going eco-evolutionary dynamics were prevented. Increased use of recalcitrant substrates was associated with parallel evolution of tctE, encoding a carbon metabolism regulator. Species interactions and species sorting set, respectively, the tempo and trajectory of evolutionary divergence among communities, selecting distinct ecological functions in otherwise equivalent ecosystems.