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      Species Interactions Alter Evolutionary Responses to a Novel Environment

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          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.


          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.

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          Most cited references 53

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          Ecological consequences of genetic diversity.

          Understanding the ecological consequences of biodiversity is a fundamental challenge. Research on a key component of biodiversity, genetic diversity, has traditionally focused on its importance in evolutionary processes, but classical studies in evolutionary biology, agronomy and conservation biology indicate that genetic diversity might also have important ecological effects. Our review of the literature reveals significant effects of genetic diversity on ecological processes such as primary productivity, population recovery from disturbance, interspecific competition, community structure, and fluxes of energy and nutrients. Thus, genetic diversity can have important ecological consequences at the population, community and ecosystem levels, and in some cases the effects are comparable in magnitude to the effects of species diversity. However, it is not clear how widely these results apply in nature, as studies to date have been biased towards manipulations of plant clonal diversity, and little is known about the relative importance of genetic diversity vs. other factors that influence ecological processes of interest. Future studies should focus not only on documenting the presence of genetic diversity effects but also on identifying underlying mechanisms and predicting when such effects are likely to occur in nature.
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            The contribution of species richness and composition to bacterial services.

            Bacterial communities provide important services. They break down pollutants, municipal waste and ingested food, and they are the primary means by which organic matter is recycled to plants and other autotrophs. However, the processes that determine the rate at which these services are supplied are only starting to be identified. Biodiversity influences the way in which ecosystems function, but the form of the relationship between bacterial biodiversity and functioning remains poorly understood. Here we describe a manipulative experiment that measured how biodiversity affects the functioning of communities containing up to 72 bacterial species constructed from a collection of naturally occurring culturable bacteria. The experimental design allowed us to manipulate large numbers of bacterial species selected at random from those that were culturable. We demonstrate that there is a decelerating relationship between community respiration and increasing bacterial diversity. We also show that both synergistic interactions among bacterial species and the composition of the bacterial community are important in determining the level of ecosystem functioning.
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              Bacteria-phage antagonistic coevolution in soil.

              Bacteria and their viruses (phages) undergo rapid coevolution in test tubes, but the relevance to natural environments is unclear. By using a "mark-recapture" approach, we showed rapid coevolution of bacteria and phages in a soil community. Unlike coevolution in vitro, which is characterized by increases in infectivity and resistance through time (arms race dynamics), coevolution in soil resulted in hosts more resistant to their contemporary than past and future parasites (fluctuating selection dynamics). Fluctuating selection dynamics, which can potentially continue indefinitely, can be explained by fitness costs constraining the evolution of high levels of resistance in soil. These results suggest that rapid coevolution between bacteria and phage is likely to play a key role in structuring natural microbial communities.

                Author and article information

                Role: Academic Editor
                PLoS Biol
                PLoS Biol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                May 2012
                May 2012
                15 May 2012
                : 10
                : 5
                [1 ]Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire, United Kingdom
                [2 ]Grantham Institute for Climate Change, Imperial College London, London, United Kingdom
                [3 ]Department of Surgery and Cancer, Faculty of Medicine, Imperial College London, London, United Kingdom
                [4 ]Department of Zoology, University of Oxford, Oxford, United Kingdom
                Cornell University, United States of America
                Author notes

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: DL TGB TB FF AP. Performed the experiments: DL VB. Analyzed the data: TGB DL TB VB JGB. Contributed reagents/materials/analysis tools: FF TB. Wrote the paper: DL TGB TB AP FF VB JGB.

                Lawrence et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 11
                Research Article
                Community Ecology
                Species Interactions
                Ecosystem Functioning
                Evolutionary Ecology
                Evolutionary Biology
                Evolutionary Processes

                Life sciences


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