Predator dispersal influences predator distribution but not prey diversity in pitcher plant microbial metacommunities.

The spatial distribution of predators can affect both the distribution and diversity of their prey. Therefore, differences in predator dispersal ability that affect their spatial distribution, could also affect prey communities. Here, we use the microbial communities within pitcher plant leaves as a model system to test the relationship between predator (protozoa) dispersal ability and distribution, and its consequences for prey (bacteria) diversity and composition. We hypothesized that limited predator dispersal results in clustered distributions and heterogeneous patches for prey species, whereas wide predator dispersal and distribution could homogenize prey metacommunities. We analyzed the distribution of two prominent bacterivore protozoans from a 2-year survey of an intact field of Sarracenia purpurea pitcher plants, and found a clustered distribution of Tetrahymena and homogeneous distribution of Poterioochromonas. We manipulated the sources of protozoan colonists and recorded protozoan recruitment and bacterial diversity in target leaves in a field experiment. We found the large ciliate, Tetrahymena, was dispersal limited and occupied few leaves, whereas the small flagellate Poterioochromonas was widely dispersed. However, the bacterial communities these protozoans feed on was unaffected by clustering of Tetrahymena, but likely influenced by Poterioochromonas and other bacterivores dispersing in the field. We propose that bacterial communities in this system are structured by a combination of well dispersed bacterivores, bacterial dispersal, and bottom-up mechanisms. Clustered predators could become strong drivers of prey communities if they were specialists or keystone predators, or if they exerted a dominant influence on other predators in top-down controlled systems. Linking dispersal ability within trophic levels and its consequences for trophic dynamics can lead to a more robust perspective on trophic metacommunities.

Nutrient dynamics in coral symbiosis depend on both the relative and absolute abundance of Symbiodiniaceae species.

BACKGROUND: Symbionts provide a variety of reproductive, nutritional, and defensive resources to their hosts, but those resources can vary depending on symbiont community composition. As genetic techniques open our eyes to the breadth of symbiont diversity within myriad microbiomes, symbiosis research has begun to consider what ecological mechanisms affect the identity and relative abundance of symbiont species and how this community structure impacts resource exchange among partners. Here, we manipulated the in hospite density and relative ratio of two species of coral endosymbionts (Symbiodinium microadriaticum and Breviolum minutum) and used stable isotope enrichment to trace nutrient exchange with the host, Briareum asbestinum. RESULTS: The patterns of uptake and translocation of carbon and nitrogen varied with both density and ratio of symbionts. Once a density threshold was reached, carbon acquisition decreased with increasing proportions of S. microadriaticum. In hosts dominated by B. minutum, nitrogen uptake was density independent and intermediate. Conversely, for those corals dominated by S. microadriaticum, nitrogen uptake decreased as densities increased, and as a result, these hosts had the overall highest (at low density) and lowest (at high density) nitrogen enrichment. CONCLUSIONS: Our findings show that the uptake and sharing of nutrients was strongly dependent on both the density of symbionts within the host, as well as which symbiont species was dominant. Together, these complex interactive effects suggest that host regulation and the repression of in hospite symbiont competition can ultimately lead to a more productive mutualism. Video Abstract.

Symbiont genotype influences holobiont response to increased temperature.

As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary rescue offers some hope for reef persistence. In tightly linked mutualisms, evolutionary rescue may occur through evolution of the host and/or endosymbionts. Many obligate mutualisms are composed of relatively small, fast-growing symbionts with greater potential to evolve on ecologically relevant time scales than their relatively large, slower growing hosts. Numerous jellyfish species harbor closely related endosymbiont taxa to other cnidarian species such as coral, and are commonly used as a model system for investigating cnidarian mutualisms. We examined the potential for adaptation of the upside-down jellyfish Cassiopea xamachana to increased temperature via evolution of its microalgal endosymbiont, Symbiodinium microadriaticum. We quantified trait variation among five algal genotypes in response to three temperatures (26 °C, 30 °C, and 32 °C) and fitness of hosts infected with each genotype. All genotypes showed positive growth rates at each temperature, but rates of respiration and photosynthesis decreased with increased temperature. Responses varied among genotypes but were unrelated to genetic similarity. The effect of temperature on asexual reproduction and the timing of development in the host also depended on the genotype of the symbiont. Natural selection could favor different algal genotypes at different temperatures, affecting host fitness. This eco-evolutionary interaction may be a critical component of understanding species resilience in increasingly stressful environments.

Individual variation in growth and physiology of symbionts in response to temperature.

In many cases, understanding species' responses to climate change requires understanding variation among individuals in response to such change. For species with strong symbiotic relationships, such as many coral reef species, genetic variation in symbiont responses to temperature may affect the response to increased ocean temperatures. To assess variation among symbiont genotypes, we examined the population dynamics and physiological responses of genotypes of Breviolum antillogorgium in response to increased temperature. We found broad temperature tolerance across genotypes, with all genotypes showing positive growth at 26, 30, and 32°C. Genotypes differed in the magnitude of the response of growth rate and carrying capacity to increasing temperature, suggesting that natural selection could favor different genotypes at different temperatures. However, the historical temperature at which genotypes were reared (26 or 30°C) was not a good predictor of contemporary temperature response. We found increased photosynthetic rates and decreased respiration rates with increasing contemporary temperature, and differences in physiology among genotypes, but found no significant differences in the response of these traits to temperature among genotypes. In species with such broad thermal tolerance, selection experiments on symbionts outside of the host may not yield results sufficient for evolutionary rescue from climate change.

Prey identity affects fitness of a generalist consumer in a brown food web.

The use of ever-advancing sequencing technologies has revealed incredible biodiversity at the microbial scale, and yet we know little about the ecological interactions in these communities. For example, in the phytotelmic community found in the purple pitcher plant, Sarracenia purpurea, ecologists typically consider the bacteria as a functionally homogenous group. In this food web, bacteria decompose detritus and are consumed by protozoa that are considered generalist consumers. Here, we tested whether a generalist consumer benefits from all bacteria equally. We isolated and identified 22 strains of bacteria, belonging to six genera, from S. purpurea plants. We grew the protozoa, Tetrahymena sp. with single isolates and strain mixtures of bacteria and measured Tetrahymena fitness. We found that different bacterial strains had different effects on protozoan fitness, both in isolation and in mixture. Our results demonstrate that not accounting for the composition of prey communities may affect the predicted outcome of predator-prey interactions.

Evolutionary responses to global change in species-rich communities.

Evolution in nature occurs in the proverbial tangled bank. The species interactions characterizing this tangled bank can be strongly affected by global change and can also influence the fitness and selective effects of a global change on a focal population. As a result, species interactions can influence which traits will promote adaptation and the magnitude or direction of evolutionary responses to the global change. First, we provide a framework describing how species interactions may influence evolutionary responses to global change. Then, we highlight case studies that have explicitly manipulated both a global change and the presence or abundance of interacting species and used either experimental evolution or quantitative genetics approaches to test for the effects of species interactions on evolutionary responses to global change. Although still not frequently considered, we argue that species interactions commonly modulate the effects of global change on the evolution of plant and animal populations. As a result, predicting the evolutionary effects of the multitude of global changes facing natural populations requires both community ecology and evolutionary perspectives.

Genetic variation in Breviolum antillogorgium, a coral reef symbiont, in response to temperature and nutrients.

Symbionts within the family Symbiodiniaceae are important on coral reefs because they provide significant amounts of carbon to many different reef species. The breakdown of this mutualism that occurs as a result of increasingly warmer ocean temperatures is a major threat to coral reef ecosystems globally. Recombination during sexual reproduction and high rates of somatic mutation can lead to increased genetic variation within symbiont species, which may provide the fuel for natural selection and adaptation. However, few studies have asked whether such variation in functional traits exists within these symbionts. We used several genotypes of two closely related species, Breviolum antillogorgium and B. minutum, to examine variation of traits related to symbiosis in response to increases in temperature or nitrogen availability in laboratory cultures. We found significant genetic variation within and among symbiont species in chlorophyll content, photosynthetic efficiency, and growth rate. Two genotypes showed decreases in traits in response to increased temperatures predicted by climate change, but one genotype responded positively. Similarly, some genotypes within a species responded positively to high-nitrogen environments, such as those expected within hosts or eutrophication associated with global change, while other genotypes in the same species responded negatively, suggesting context-dependency in the strength of mutualism. Such variation in traits implies that there is potential for natural selection on symbionts in response to temperature and nutrients, which could confer an adaptive advantage to the holobiont.

Pick your trade-offs wisely: Predator-prey eco-evo dynamics are qualitatively different under different trade-offs.

In recent decades, myriad studies have explored the population dynamics of coevolving populations of predator and prey. A variety of choices are made in these models: exponential or logistic prey growth in the absence of a predator, various forms of predator functional response, and uni- or bi-directional trait axes. In addition, some form of trade-offs are assumed in order to prevent run-away evolution of the prey and predator traits. While there is a considerable amount of theory regarding various forms of prey growth rates and predator functional responses, only a few studies have explored how different types of trade-offs affect predator-prey dynamics. Here, we compared two ditrophic coevolution models incorporating different trade-offs via dual effects of the prey trait on attack rate and either prey carrying capacity or intrinsic growth rate. We employed a standard dynamical systems approach to analyze the equilibrium conditions of each model and find conditions for non-equilibrium oscillatory coexistence. The exact effect of various parameters on the outcome of predator-prey interactions depends on whether the trade-offs affect the intrinsic growth rate or carrying capacity. In particular, coexistence is more likely when prey growth rate is affected by the evolving trait. In addition, in parameter regimes where cycles occur in both models, oscillations typically have larger periods and amplitudes when prey growth rate is affected by the evolving trait.

Genetic variation in mutualistic and antagonistic interactions in an invasive legume.

Mutualists may play an important role in invasion success. The ability to take advantage of novel mutualists or survive and reproduce despite a lack of mutualists may facilitate invasion by those individuals with such traits. Here, we used two greenhouse studies to examine how soil microbial communities in general and mutualistic rhizobia in particular affect the performance of a legume species (Medicago polymorpha) that has invaded five continents. We performed two plant growth experiments with Medicago polymorpha, inoculating them with soil slurries in one experiment or rhizobial cultures in another experiment. For both experiments, we compared the growth of Medicago in competition with conspecific or heterospecific plants and examined variation among plant genotypes collected from the native and introduced ranges. We found that all genotypes experienced similar increases in biomass and formed more nodules that house rhizobia bacteria when inoculated with soil from a previously invaded site, compared to uninoculated plants or plants inoculated with soil from uninvaded and low invasion sites. In a second experiment, plants inoculated with rhizobia generally produced more biomass, had greater tolerance to interspecific competition, and had greater effects on competitor biomass than uninoculated plants. However, plant genotypes collected from the native range benefited more from rhizobia and were less tolerant of competition relative to genotypes collected from the introduced range. In the introduced range, compatible mutualists may not be readily available but competition is intense, causing Medicago to evolve to benefit less from interactions with rhizobia mutualists, while simultaneously becoming more tolerant of competition.

Evolution of increased Medicaco polymorpha size during invasion does not result in increased competitive ability.

Species invading new habitats experience novel selection pressures that can lead to rapid evolution, which may contribute to invasion success and/or increased impact on native community members. Many studies have hypothesized that plants in the introduced range will be larger than those in the native range, leading to increases in competitive ability. There is mixed support for evolution of larger sizes in the introduced range, but few studies have explicitly tested whether evolutionary changes result in decreased competitive responses or increased competitive effects on other species in the community. Here, we show that introduced Medicago polymorpha genotypes produced 14% more aboveground and 41% more belowground biomass than genotypes from the native range, suggesting that evolutionary changes in size occurred after introduction. However, these size differences were only observed in the absence of competition. The competitive effects of introduced and native range genotypes on three species that commonly co-occur with Medicago in invaded regions were remarkably similar. These results suggest that evolutionary increases in size during biological invasions do not necessarily alter the competitive effects of the invader on other community members, but may increase invasion success in disturbed or low competition environments.

Testing genotypic variation of an invasive plant species in response to soil disturbance and herbivory.

Herbivores, competitors, and predators can inhibit biological invasions ("biotic resistance" sensu Elton 1959), while disturbance typically promotes biological invasions. Although biotic resistance and disturbance are often considered separately in the invasion literature, these two forces may be linked. One mechanism by which disturbance may facilitate biological invasions is by decreasing the effectiveness of biotic resistance. The effects of both disturbance and biotic resistance may vary across invading genotypes, and genetic variation in the invasive propagule pool may increase the likelihood that some genotypes can overcome biotic resistance or take greater advantage of disturbance. We conducted an experimental field trial in which we manipulated soil disturbance (thatch removal and loosening soil) and the presence of insect herbivores and examined their effects on the invasion success of 44 Medicago polymorpha genotypes. As expected, insecticide reduced leaf damage and increased Medicago fecundity, suggesting that insect herbivores in this system provide some biotic resistance. Soil disturbance increased Medicago fecundity, but did not alter the effectiveness of biotic resistance by insect herbivores. We found significant genetic variation in Medicago in response to disturbance, but not in response to insect herbivores. These results suggest that the ability of Medicago to invade particular habitats depends on the amount of insect herbivory, the history of disturbance in the habitat, and how the specific genotypes in the invader pool respond to these factors.

A shift from exploitation to interference competition with increasing density affects population and community dynamics.

Intraspecific competition influences population and community dynamics and occurs via two mechanisms. Exploitative competition is an indirect effect that occurs through use of a shared resource and depends on resource availability. Interference competition occurs by obstructing access to a resource and may not depend on resource availability. Our study tested whether the strength of interference competition changes with protozoa population density. We grew experimental microcosms of protozoa and bacteria under different combinations of protozoan density and basal resource availability. We then solved a dynamic predator-prey model for parameters of the functional response using population growth rates measured in our experiment. As population density increased, competition shifted from exploitation to interference, and competition was less dependent on resource levels. Surprisingly, the effect of resources was weakest when competition was the most intense. We found that at low population densities, competition was largely exploitative and resource availability had a large effect on population growth rates, but the effect of resources was much weaker at high densities. This shift in competitive mechanism could have implications for interspecific competition, trophic interactions, community diversity, and natural selection. We also tested whether this shift in the mechanism of competition with protozoa density affected the structure of the bacterial prey community. We found that both resources and protozoa density affected the structure of the bacterial prey community, suggesting that competitive mechanism may also affect trophic interactions.

Quantifying nonadditive selection caused by indirect ecological effects.

In natural biological communities, species interact with many other species. Multiple species interactions can lead to indirect ecological effects that have important fitness consequences and can cause nonadditive patterns of natural selection. Given that indirect ecological effects are common in nature, nonadditive selection may also be quite common. As a result, quantifying nonadditive selection resulting from indirect ecological effects may be critical for understanding adaptation in natural communities composed of many interacting species. We describe how to quantify the relative strength of nonadditive selection resulting from indirect ecological effects compared to the strength of pairwise selection. We develop a clear method for testing for nonadditive selection caused by indirect ecological effects and consider how it might affect adaptation in multispecies communities. We use two case studies to illustrate how our method can be applied to empirical data sets. Our results suggest that nonadditive selection caused by indirect ecological effects may be common in nature. Our hope is that trait-based approaches, combined with multifactorial experiments, will result in more estimates of nonadditive selection that reveal the relative importance of indirect ecological effects for evolution in a community context.

Causes and consequences of failed adaptation to biological invasions: the role of ecological constraints.

Biological invasions are a major challenge to native communities and have the potential to exert strong selection on native populations. As a result, native taxa may adapt to the presence of invaders through increased competitive ability, increased antipredator defences or altered morphologies that may limit encounters with toxic prey. Yet, in some cases, species may fail to adapt to biological invasions. Many challenges to adaptation arise because biological invasions occur in complex species-rich communities in spatially and temporally variable environments. Here, we review these 'ecological' constraints on adaptation, focusing on the complications that arise from the need to simultaneously adapt to multiple biotic agents and from temporal and spatial variation in both selection and demography. Throughout, we illustrate cases where these constraints might be especially important in native populations faced with biological invasions. Our goal was to highlight additional complexities empiricists should consider when studying adaptation to biological invasions and to begin to identify conditions when adaptation may fail to be an effective response to invasion.

Rethinking niche evolution: experiments with natural communities of Protozoa in pitcher plants.

Classic niche theory predicts that competing species will evolve to use different resources and interact less, whereas recent niche-converge ideas predict that species evolve to use similar resources and interact more. Most data supporting niche evolution are based on observations of contemporary niche use, whereas experimental support is quite sparse. We followed the evolution of four species of Protozoa during succession in the water-filled leaves of the pitcher plant, Sarracenia purpurea, and found that evolution in multispecies systems follows a surprising pattern. Over several hundred generations, weak competitors evolved to be stronger, while strong competitors evolved to become weaker, which does not conform to expectations of either niche divergence or convergence. Evolution in this system appears to occur in response to characteristics of a suite of several competitors in the community, rather than pairwise interactions. Ecologists may need to rethink the roles of competition and evolution in structuring communities.

The relative importance of rapid evolution for plant-microbe interactions depends on ecological context.

Evolution can occur on ecological time-scales, affecting community and ecosystem processes. However, the importance of evolutionary change relative to ecological processes remains largely unknown. Here, we analyse data from a long-term experiment in which we allowed plant populations to evolve for three generations in dry or wet soils and used a reciprocal transplant to compare the ecological effect of drought and the effect of plant evolutionary responses to drought on soil microbial communities and nutrient availability. Plants that evolved under drought tended to support higher bacterial and fungal richness, and increased fungal : bacterial ratios in the soil. Overall, the magnitudes of ecological and evolutionary effects on microbial communities were similar; however, the strength and direction of these effects depended on the context in which they were measured. For example, plants that evolved in dry environments increased bacterial abundance in dry contemporary environments, but decreased bacterial abundance in wet contemporary environments. Our results suggest that interactions between recent evolutionary history and ecological context affect both the direction and magnitude of plant effects on soil microbes. Consequently, an eco-evolutionary perspective is required to fully understand plant-microbe interactions.

Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities.

Succession is a foundation concept in ecology that describes changes in species composition through time, yet many successional patterns have not been thoroughly investigated. We highlight three hypotheses about succession that are often not clearly stated or tested: (1) individual communities become more stable over time, (2) replicate communities become more similar over time, and (3) diversity peaks at mid-succession. Testing general patterns of succession requires estimates of variation in trajectories within and among replicate communities. We followed replicate aquatic communities found within leaves of purple pitcher plants (Sarracenia purpurea) to test these three hypotheses. We found that stability of individual communities initially decreased, but then increased in older communities. Predation was highest in younger leaves but then declined, while competition was likely strongest in older leaves, as resources declined through time. Higher levels of predation and competition corresponded with periods of higher stability. As predicted, heterogeneity among communities decreased with age, suggesting that communities became more similar over time. Changes in diversity depended on trophic level. The diversity of bacteria slightly declined over time, but the diversity of consumers of bacteria increased linearly and strongly throughout succession. We suggest that studies need to focus on the variety of environmental drivers of succession, which are likely to vary through time and across habitats.

Evolution in response to direct and indirect ecological effects in pitcher plant inquiline communities.

Ecologists have long recognized the importance of indirect ecological effects on species abundances, coexistence, and diversity. However, the evolutionary consequences of indirect interactions are rarely considered. Here I conduct selection experiments and examine the evolutionary response of Colpoda sp., a ciliated protozoan, to other members of the inquiline community of purple pitcher plants (Sarracenia purpurea). I measured the evolution of six traits in response to (1) predation by mosquito larvae, (2) competition from other ciliated protozoans, and (3) simultaneous predation and competition. The latter treatment incorporated both direct effects and indirect effects due to interactions between predators and competitors. Population growth rate and cell size evolved in response to direct effects of predators and competitors. However, trait values in the multispecies treatment were similar to those in the monoculture treatment, indicating that direct effects were offset by strong indirect effects on the evolution of traits. For most of the traits measured, indirect effects were opposed to, and often stronger than, direct effects. These indirect effects occurred as a result of behavioral changes of the predator in the presence of competitors and as a result of reduced densities of competitors in the presence of predators. Incorporating indirect effects provides a more realistic description of how species evolve in complex natural communities.