Contemporary evolution rivals the effects of rhizobium presence on community and ecosystem properties in experimental mesocosms.

Because genotypes within a species commonly differ in traits that influence other species, whole communities, or even ecosystem functions, evolutionary change within one key species may affect the community and ecosystem processes. Here we use experimental mesocosms to test how the evolution of reduced cooperation in rhizobium mutualists in response to 20 years of nitrogen fertilization compares to the effects of rhizobium presence on soil nitrogen availability and plant community composition and diversity. The evolution of reduced rhizobium cooperation caused reductions in soil nitrogen, biological nitrogen fixation, and leaf nitrogen concentrations that were as strong as, or even stronger than, experimental rhizobium inoculation (presence/absence) treatments. Effects of both rhizobium evolution and rhizobium inoculation on legume dominance, plant community composition, and plant species diversity were often smaller in magnitude, but suggest that rhizobium evolution can alter the relative abundance of plant functional groups. Our findings indicate that the consequences of rapid microbial evolution for ecosystems and communities can rival the effects resulting from the presence or abundance of keystone mutualists.

Light availability and rhizobium variation interactively mediate the outcomes of legume-rhizobium symbiosis.

PREMISE: Nutrients, light, water, and temperature are key factors limiting the growth of individual plants in nature. Mutualistic interactions between plants and microbes often mediate resource limitation for both partners. In the mutualism between legumes and rhizobia, plants provide rhizobia with carbon in exchange for fixed nitrogen. Because partner quality in mutualisms is genotype-dependent, within-species genetic variation is expected to alter the responses of mutualists to changes in the resource environment. Here we ask whether partner quality variation in rhizobia mediates the response of host plants to changing light availability, and conversely, whether light alters the expression of partner quality variation. METHODS: We inoculated clover hosts with 11 strains of Rhizobium leguminosarum that differed in partner quality, grew plants under either ambient or low light conditions in the greenhouse, and measured plant growth, nodule traits, and foliar nutrient composition. RESULTS: Light availability and rhizobium inoculum interactively determined plant growth, and variation in rhizobium partner quality was more apparent in ambient light. CONCLUSIONS: Our results suggest that variation in the costs and benefits of rhizobium symbionts mediate host responses to light availability and that rhizobium strain variation might more important in higher-light environments. Our work adds to a growing appreciation for the role of microbial intraspecific and interspecific diversity in mediating extended phenotypes in their hosts and suggests an important role for light availability in the ecology and evolution of legume-rhizobium symbiosis.

Long-term agricultural management does not alter the evolution of a soybean-rhizobium mutualism.

Leguminous crops, like soybeans, often rely on biologically fixed nitrogen via their symbiosis with rhizobia rather than synthetic nitrogen inputs. However, agricultural management practices may influence the effectiveness of biological nitrogen fixation (BNF). While the ecological effects of agricultural management on rhizobia have received some attention, the evolutionary effects have been neglected in comparison. Resource mutualism theory predicts that evolutionary effects are likely, however. Both fertilization and tillage are predicted to cause the evolution of rhizobia that provide fewer growth benefits to plant hosts and fix less nitrogen. This study capitalized on a Long-Term Ecological Research experiment that manipulated agricultural management practices in a corn-soybean-wheat row crop system for 24 yr to investigate whether four different management practices (conventional, no-till, low chemical input, and certified organic) cause rhizobia populations to evolve to become more or less cooperative. We found little evidence that 24 yr of varying management practices affect the net growth benefits rhizobia provide to soybeans, although soybean plants inoculated with soils collected from conventional treatments tended to have lower BNF rates than plants inoculated with soils from the no-till, low input, and organic management treatments. These findings suggest that rhizobia will continue to provide adequate growth benefits to leguminous crops in the future, even in intensively managed systems.

Decoupled genomic elements and the evolution of partner quality in nitrogen-fixing rhizobia.

Understanding how mutualisms evolve in response to a changing environment will be critical for predicting the long-term impacts of global changes, such as increased N (nitrogen) deposition. Bacterial mutualists in particular might evolve quickly, thanks to short generation times and the potential for independent evolution of plasmids through recombination and/or HGT (horizontal gene transfer). In a previous work using the legume/rhizobia mutualism, we demonstrated that long-term nitrogen fertilization caused the evolution of less-mutualistic rhizobia. Here, we use our 63 previously isolated rhizobium strains in comparative phylogenetic and quantitative genetic analyses to determine the degree to which variation in partner quality is attributable to phylogenetic relationships among strains versus recent genetic changes in response to N fertilization. We find evidence of distinct evolutionary relationships between chromosomal and pSym genes, and broad similarity between pSym genes. We also find that nifD has a unique evolutionary history that explains much of the variation in partner quality, and suggest MoFe subunit interaction sites in the evolution of less-mutualistic rhizobia. These results provide insight into the mechanisms behind the evolutionary response of rhizobia to long-term N fertilization, and we discuss the implications of our results for the evolution of the mutualism.

Long-term nitrogen addition causes the evolution of less-cooperative mutualists.

Human activities have altered the global nitrogen (N) cycle, and as a result, elevated N inputs are causing profound ecological changes in diverse ecosystems. The evolutionary consequences of this global change have been largely ignored even though elevated N inputs are predicted to cause mutualism breakdown and the evolution of decreased cooperation between resource mutualists. Using a long-term (22 years) N-addition experiment, we find that elevated N inputs have altered the legume-rhizobium mutualism (where rhizobial bacteria trade N in exchange for photosynthates from legumes), causing the evolution of less-mutualistic rhizobia. Plants inoculated with rhizobium strains isolated from N-fertilized treatments produced 17-30% less biomass and had reduced chlorophyll content compared to plants inoculated with strains from unfertilized control plots. Because the legume-rhizobium mutualism is the major contributor of naturally fixed N to terrestrial ecosystems, the evolution of less-cooperative rhizobia may have important environmental consequences.

Contemporary and historical evolutionary processes interact to shape patterns of within-lake phenotypic divergences in polyphenic pumpkinseed sunfish, Lepomis gibbosus.

Historical and contemporary evolutionary processes can both contribute to patterns of phenotypic variation among populations of a species. Recent studies are revealing how interactions between historical and contemporary processes better explain observed patterns of phenotypic divergence than either process alone. Here, we investigate the roles of evolutionary history and adaptation to current environmental conditions in structuring phenotypic variation among polyphenic populations of sunfish inhabiting 12 postglacial lakes in eastern North America. The pumpkinseed sunfish polyphenism includes sympatric ecomorphs specialized for littoral or pelagic lake habitats. First, we use population genetic methods to test the evolutionary independence of within-lake phenotypic divergences of ecomorphs and to describe patterns of genetic structure among lake populations that clustered into three geographical groupings. We then used multivariate analysis of covariance (MANCOVA) to partition body shape variation (quantified with geometric morphometrics) among the effects of evolutionary history (reflecting phenotypic variation among genetic clusters), the shared phenotypic response of all populations to alternate habitats within lakes (reflecting adaptation to contemporary conditions), and unique phenotypic responses to habitats within lakes nested within genetic clusters. All effects had a significant influence on body form, but the effects of history and the interaction between history and contemporary habitat were larger than contemporary processes in structuring phenotypic variation. This highlights how divergence can be better understood against a known backdrop of evolutionary history.

Eco-evolutionary effects on population recovery following catastrophic disturbance.

Fine-scale genetic diversity and contemporary evolution can theoretically influence ecological dynamics in the wild. Such eco-evolutionary effects might be particularly relevant to the persistence of populations facing acute or chronic environmental change. However, experimental data on wild populations is currently lacking to support this notion. One way that ongoing evolution might influence the dynamics of threatened populations is through the role that selection plays in mediating the 'rescue effect', the ability of migrants to contribute to the recovery of populations facing local disturbance and decline. Here, we combine experiments with natural catastrophic events to show that ongoing evolution is a major determinant of migrant contributions to population recovery in Trinidadian guppies (Poecilia reticulata). These eco-evolutionary limits on migrant contributions appear to be mediated by the reinforcing effects of natural and sexual selection against migrants, despite the close geographic proximity of migrant sources. These findings show that ongoing adaptive evolution can be a double-edged sword for population persistence, maintaining local fitness at a cost to demographic risk. Our study further serves as a potent reminder that significant evolutionary and eco-evolutionary dynamics might be at play even where the phenotypic status quo is largely maintained generation to generation.

Both geography and ecology contribute to mating isolation in guppies.

Local adaptation to different environments can promote mating isolation--either as an incidental by-product of trait divergence, or as a result of selection to avoid maladaptive mating. Numerous recent empirical examples point to the common influence of divergent natural selection on speciation based largely on evidence of strong pre-mating isolation between populations from different habitat types. Accumulating evidence for natural selection's influence on speciation is therefore no longer a challenge. The difficulty, rather, is in determining the mechanisms involved in the progress of adaptive divergence to speciation once barriers to gene flow are already present. Here, we present results of both laboratory and field experiments with Trinidadian guppies (Poecilia reticulata) from different environments, who do not show complete reproductive isolation despite adaptive divergence. We investigate patterns of mating isolation between populations that do and do not exchange migrants and show evidence for both by-product and reinforcement mechanisms depending on female ecology. Specifically, low-predation females discriminate against all high-predation males thus implying a by-product mechanism, whereas high-predation females only discriminate against low-predation males from further upstream in the same river, implying selection to avoid maladaptive mating. Our study thus confirms that mechanisms of adaptive speciation are not necessarily mutually exclusive and uncovers the complex ecology-geography interactions that underlie the evolution of mating isolation in nature.

Spatiotemporal variation in linear natural selection on body color in wild guppies (Poecilia reticulata).

We conducted 10 mark-recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low-predation sites than in high-predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low-predation experiments. Instead, some of the most intense bouts of selection against color occurred in low-predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.

Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams.

Evolution has been shown to be a critical determinant of ecological processes in some systems, but its importance relative to traditional ecological effects is not well known. In addition, almost nothing is known about the role of coevolution in shaping ecosystem function. Here, we experimentally evaluated the relative effects of species invasion (a traditional ecological effect), evolution and coevolution on ecosystem processes in Trinidadian streams. We manipulated the presence and population-of-origin of two common fish species, the guppy (Poecilia reticulata) and the killifish (Rivulus hartii). We measured epilithic algal biomass and accrual, aquatic invertebrate biomass, and detrital decomposition. Our results show that, for some ecosystem responses, the effects of evolution and coevolution were larger than the effects of species invasion. Guppy evolution in response to alternative predation regimes significantly influenced algal biomass and accrual rates. Guppies from a high-predation site caused an increase in algae relative to guppies from a low-predation site; algae effects were probably shaped by observed divergence in rates of nutrient excretion and algae consumption. Rivulus-guppy coevolution significantly influenced the biomass of aquatic invertebrates. Locally coevolved populations reduced invertebrate biomass relative to non-coevolved populations. These results challenge the general assumption that intraspecific diversity is a less critical determinant of ecosystem function than is interspecific diversity. Given existing evidence for contemporary evolution in these fish species, our findings suggest considerable potential for eco-evolutionary feedbacks to operate as populations adapt to natural or anthropogenic perturbations.

Adaptive changes in life history and survival following a new guppy introduction.

Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life-history traits and survival rates for wild guppies introduced into new environments. Female life-history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment.