Caroline B. Turner

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.

Sustained fitness gains and variability in fitness trajectories in the long-term evolution experiment with Escherichia coli

Many populations live in environments subject to frequent biotic and abiotic changes. Nonetheless, it is interesting to ask whether an evolving populations mean fitness can increase indefinitely, and potentially without any limit, even in a constant environment. A recent study showed that fitness trajectories of Escherichia coli populations over 50 000 generations were better described by a power-law model than by a hyperbolic model. According to the power-law model, the rate of fitness gain declines over time but fitness has no upper limit, whereas the hyperbolic model implies a hard limit. Here, we examine whether the previously estimated power-law model predicts the fitness trajectory for an additional 10 000 generations. To that end, we conducted more than 1100 new competitive fitness assays. Consistent with the previous study, the power-law model fits the new data better than the hyperbolic model. We also analysed the variability in fitness among populations, finding subtle, but significant, heterogeneity in mean fitness. Some, but not all, of this variation reflects differences in mutation rate that evolved over time. Taken together, our results imply that both adaptation and divergence can continue indefinitely—or at least for a long time—even in a constant environment.

Full title: Evolution and coexistence in response to a key innovation in a long-term evolution experiment with Escherichia coli

Evolution of a novel function can greatly alter the effects of an organism on its environment. These environmental changes can, in turn, affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following evolution of a novel function in the long-term evolution experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to consume citrate aerobically. However, that ability evolved in one of the LTEE populations. In this population, citrate-utilizing bacteria (Cit+) coexisted stably with another clade of bacteria that lacked the capacity to utilize citrate (Cit−). This coexistence was shaped by the evolution of a cross-feeding relationship in which Cit+ cells released the dicarboxylic acids succinate, fumarate, and malate into the medium, and Cit− cells evolved improved growth on these carbon sources, as did the Cit+ cells. Thus, the evolution of citrate consumption led to a flask-based ecosystem that went from a single limiting resource, glucose, to one with five resources either shared or partitioned between two coexisting clades. Our findings show how evolutionary novelties can change environmental conditions, thereby facilitating diversity and altering both the structure of an ecosystem and the evolutionary trajectories of coexisting organisms. Evolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one. –Francois Jacob

Replaying Evolution to Test the Cause of Extinction of One Ecotype in an Experimentally Evolved Population

In a long-term evolution experiment with Escherichia coli, bacteria in one of twelve populations evolved the ability to consume citrate, a previously unexploited resource in a glucose-limited medium. This innovation led to the frequency-dependent coexistence of citrate-consuming (Cit+) and non-consuming (Cit–) ecotypes, with Cit−bacteria persisting on the exogenously supplied glucose as well as other carbon molecules released by the Cit+ bacteria. After more than 10,000 generations of coexistence, however, the Cit−lineage went extinct; cells with the Cit−phenotype dropped to levels below detection, and the Cit−clade could not be detected by molecular assays based on its unique genotype. We hypothesized that this extinction was a deterministic outcome of evolutionary change within the population, specifically the appearance of a more-fit Cit+ ecotype that competitively excluded the Cit−ecotype. We tested this hypothesis by re-evolving the population from a frozen population sample taken within 500 generations of the extinction and from another sample taken several thousand generations earlier, in each case for 500 generations and with 20-fold replication. To our surprise, the Cit−type did not go extinct in any of these replays, and Cit−cells also persisted in a single replicate that was propagated for 2,500 generations. Even more unexpectedly, we showed that the Cit−ecotype could reinvade the Cit+ population after its extinction. Taken together, these results indicate that the extinction of the Cit−ecotype was not a deterministic outcome driven by competitive exclusion by the Cit+ ecotype. The extinction also cannot be explained by demographic stochasticity alone, as the population size of the Cit−ecotype should have been many thousands of cells even during the daily transfer events. Instead, we infer that the extinction must have been caused by a rare chance event in which some aspect of the experimental conditions was inadvertently perturbed.

A global database of nitrogen and phosphorus excretion rates of aquatic animals

Animals can be important in modulating ecosystem-level nutrient cycling, although their importance varies greatly among species and ecosystems. Nutrient cycling rates of individual animals represent valuable data for testing the predictions of important frameworks such as the Metabolic Theory of Ecology (MTE) and ecological stoichiometry (ES). They also represent an important set of functional traits that may reflect both environmental and phylogenetic influences. Over the past two decades, studies of animal-mediated nutrient cycling have increased dramatically, especially in aquatic ecosystems. Here we present a global compilation of aquatic animal nutrient excretion rates. The dataset includes 10,534 observations from freshwater and marine animals of N and/or P excretion rates. These observations represent 491 species, including most aquatic phyla. Coverage varies greatly among phyla and other taxonomic levels. The dataset includes information on animal body size, ambient temperature, taxonomic affiliations, and animal body N:P. This data set was used to test predictions of MTE and ES, as described in Vanni and McIntyre (2016; Ecology DOI: 10.1002/ecy.1582).

Evolution of organismal stoichiometry in a 50,000-generation experiment with Escherichia coli

Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, little is known about rates and directions of evolutionary changes in elemental composition in response to nutrient limitation. We measured carbon, nitrogen, and phosphorus content of Escherichia coli evolved under controlled carbon-limited conditions for 50,000 generations. The bacteria evolved higher relative nitrogen and phosphorus content, consistent with selection for increased use of the more abundant elements. Total carbon assimilated also increased, indicating more efficient use of the limiting element. Altogether, our study shows that stoichiometry evolved over a relatively short time-period, and that it did so in a predictable direction given the carbon-limiting environment.

Evolution of organismal stoichiometry in a long-term experiment with Escherichia coli

Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, much less is known about the rates and directions of evolutionary changes in elemental composition. We measured carbon, nitrogen and phosphorus content of 12 Escherichia coli populations that evolved under controlled carbon-limited, serial-transfer conditions for 50 000 generations. The bacteria evolved higher relative nitrogen and phosphorus content, consistent with selection for increased use of the more abundant elements. Total carbon assimilated also increased, indicating more efficient use of the limiting element. We also measured stoichiometry in one population repeatedly through time. Stoichiometry changed more rapidly in early generations than later on, similar to the trajectory seen for competitive fitness. Altogether, our study shows that stoichiometry evolved over long time periods, and that it did so in a predictable direction, given the carbon-limited environment.

Parallel genetic adaptation across environments differing in mode of growth or resource availability

Evolution experiments have demonstrated high levels of genetic parallelism between populations evolving in identical environments. However, natural populations evolve in complex environments that can vary in many ways, likely sharing some characteristics but not others. Here, we ask whether shared selection pressures drive parallel evolution across distinct environments. We addressed this question in experimentally evolved populations founded from a clone of the bacterium Burkholderia cenocepacia. These populations evolved for 90 days (approximately 600 generations) under all combinations of high or low carbon availability and selection for either planktonic or biofilm modes of growth. Populations that evolved in environments with shared selection pressures (either level of carbon availability or mode of growth) were more genetically similar to each other than populations from environments that shared neither characteristic. However, not all shared selection pressures led to parallel evolution. Genetic parallelism between low‐carbon biofilm and low‐carbon planktonic populations was very low despite shared selection for growth under low‐carbon conditions, suggesting that evolution in low‐carbon environments may generate stronger trade‐offs between biofilm and planktonic modes of growth. For all environments, a populations fitness in a particular environment was positively correlated with the genetic similarity between that population and the populations that evolved in that particular environment. Although genetic similarity was low between low‐carbon environments, overall, evolution in similar environments led to higher levels of genetic parallelism and that genetic parallelism, in turn, was correlated with fitness in a particular environment.