Species Interactions Alter Evolutionary Responses to a Novel Environment

Abstract

Adaptation to a novel environment is altered by the presence of co-occurring species. Species in diverse communities evolved complementary resource use, which altered the functioning of the experimental ecosystems.

Abstract

Studies of evolutionary responses to novel environments typically consider single species or perhaps pairs of interacting species. However, all organisms co-occur with many other species, resulting in evolutionary dynamics that might not match those predicted using single species approaches. Recent theories predict that species interactions in diverse systems can influence how component species evolve in response to environmental change. In turn, evolution might have consequences for ecosystem functioning. We used experimental communities of five bacterial species to show that species interactions have a major impact on adaptation to a novel environment in the laboratory. Species in communities diverged in their use of resources compared with the same species in monocultures and evolved to use waste products generated by other species. This generally led to a trade-off between adaptation to the abiotic and biotic components of the environment, such that species evolving in communities had lower growth rates when assayed in the absence of other species. Based on growth assays and on nuclear magnetic resonance (NMR) spectroscopy of resource use, all species evolved more in communities than they did in monocultures. The evolutionary changes had significant repercussions for the functioning of these experimental ecosystems: communities reassembled from isolates that had evolved in polyculture were more productive than those reassembled from isolates that had evolved in monoculture. Our results show that the way in which species adapt to new environments depends critically on the biotic environment of co-occurring species. Moreover, predicting how functioning of complex ecosystems will respond to an environmental change requires knowing how species interactions will evolve.

Author Summary

Understanding how species adapt to new environments is important both for evolutionary theory and for predicting and managing ecosystem responses to changing environments. However, most research into adaptation to new environments has considered species in isolation. Whether results from these systems apply to more realistically diverse groups of species remains unclear. We exposed five species of bacteria, collected from pools around the roots of beech trees, to a novel laboratory environment either in isolation or in species mixtures for approximately 70 generations. We found that each species evolved more in diverse species mixtures than it did when cultured in isolation. Moreover, species diverged in their use of resources and how they used the waste products of other species. These changes meant that the community of bacteria that evolved together used more of the available resources and were thereby more productive than the same group of species that evolved in isolation. Our findings show that species interactions can have a major effect on evolutionary dynamics, which can in turn influence ecosystem functioning.