Trophic interactions in microbiomes influence plant host population size and ecosystem function.

Plant microbiomes that comprise diverse microorganisms, including prokaryotes, eukaryotes and viruses, are the key determinants of plant population dynamics and ecosystem function. Despite their importance, little is known about how species interactions (especially trophic interactions) between microbes from different domains modify the importance of microbiomes for plant hosts and ecosystems. Using the common duckweed Lemna minor, we experimentally examined the effects of predation (by bacterivorous protists) and parasitism (by bacteriophages) within microbiomes on plant population size and ecosystem phosphorus removal. Our results revealed that the addition of predators increased plant population size and phosphorus removal, whereas the addition of parasites showed the opposite pattern. The structural equation modelling further pointed out that predation and parasitism affected plant population size and ecosystem function via distinct mechanisms that were both mediated by microbiomes. Our results highlight the importance of understanding microbial trophic interactions for predicting the outcomes and ecosystem impacts of plant-microbiome symbiosis.

Neopolyploidy-induced changes in giant duckweed (Spirodela polyrhiza) alter herbivore preference and performance and plant population performance.

PREMISE: Polyploidy is a widespread mutational process in angiosperms that may alter population performance of not only plants but also their interacting species. Yet, knowledge of whether polyploidy affects plant-herbivore dynamics is scarce. Here, we tested whether aphid herbivores exhibit preference for diploid or neopolyploid plants, whether polyploidy impacts plant and herbivore performance, and whether these interactions depend on the plant genetic background. METHODS: Using independently synthesized neotetraploid strains paired with their diploid progenitors of greater duckweed (Spirodela polyrhiza), we evaluated the effect of neopolyploidy on duckweed's interaction with the water-lily aphid (Rhopalosiphum nymphaeae). Using paired-choice experiments, we evaluated feeding preference of the herbivore. We then evaluated the consequences of polyploidy on aphid and plant performance by measuring population growth over multiple generations. RESULTS: Aphids preferred neopolyploids when plants were provided at equal abundances but not at equal surface areas, suggesting the role of plant population surface area in driving this preference. Additionally, neopolyploidy increased aphid population performance, but this result was dependent on the plant's genetic lineage. Lastly, the impact of herbivory on neopolyploid vs. diploid duckweed varied greatly with genetic lineage, where neopolyploids appeared to be variably tolerant compared to diploids, sometimes mirroring the effect on herbivore performance. CONCLUSIONS: By experimentally testing the impacts of polyploidy on trophic species interactions, we showed that polyploidization can impact the preference and performance of herbivores on their plant hosts. These results have significant implications for the establishment and persistence of plants and herbivores in the face of plant polyploidy.

Polyploidy impacts population growth and competition with diploids: multigenerational experiments reveal key life-history trade-offs.

Ecological theory predicts that early generation polyploids ('neopolyploids') should quickly go extinct owing to the disadvantages of rarity and competition with their diploid progenitors. However, polyploids persist in natural habitats globally. This paradox has been addressed theoretically by recognizing that reproductive assurance of neopolyploids and niche differentiation can promote establishment. Despite this, the direct effects of polyploidy at the population level remain largely untested despite establishment being an intrinsically population-level process. We conducted population-level experiments where life-history investment in current and future growth was tracked in four lineage pairs of diploids and synthetic autotetraploids of the aquatic plant Spirodela polyrhiza. Population growth was evaluated with and without competition between diploids and neopolyploids across a range of nutrient treatments. Although neopolyploid populations produce more biomass, they reach lower population sizes and have reduced carrying capacities when growing alone or in competition across all nutrient treatments. Thus, contrary to individual-level studies, our population-level data suggest that neopolyploids are competitively inferior to diploids. Conversely, neopolyploid populations have greater investment in dormant propagule production than diploids. Our results show that neopolyploid populations should not persist based on current growth dynamics, but high potential future growth may allow polyploids to establish in subsequent seasons.

Plant neopolyploidy and genetic background differentiate the microbiome of duckweed across a variety of natural freshwater sources.

Whole-genome duplication has long been appreciated for its role in driving phenotypic novelty in plants, often altering the way organisms interface with the abiotic environment. Only recently, however, have we begun to investigate how polyploidy influences interactions of plants with other species, despite the biotic niche being predicted as one of the main determinants of polyploid establishment. Nevertheless, we lack information about how polyploidy affects the diversity and composition of the microbial taxa that colonize plants, and whether this is genotype-dependent and repeatable across natural environments. This information is a first step towards understanding whether the microbiome contributes to polyploid establishment. We, thus, tested the immediate effect of polyploidy on the diversity and composition of the bacterial microbiome of the aquatic plant Spirodela polyrhiza using four pairs of diploids and synthetic autotetraploids. Under controlled conditions, axenic plants were inoculated with pond waters collected from 10 field sites across a broad environmental gradient. Autotetraploids hosted 4%-11% greater bacterial taxonomic and phylogenetic diversity than their diploid progenitors. Polyploidy, along with its interactions with the inoculum source and genetic lineage, collectively explained 7% of the total variation in microbiome composition. Furthermore, polyploidy broadened the core microbiome, with autotetraploids having 15 unique bacterial taxa in addition to the 55 they shared with diploids. Our results show that whole-genome duplication directly leads to novelty in the plant microbiome and importantly that the effect is dependent on the genetic ancestry of the polyploid and generalizable over many environmental contexts.

Effects of rapid evolution on species coexistence.

Increasing evidence for rapid evolution suggests that the maintenance of species diversity in ecological communities may be influenced by more than purely ecological processes. Classic theory shows that interspecific competition may select for traits that increase niche differentiation, weakening competition and thus promoting species coexistence. While empirical work has demonstrated trait evolution in response to competition, if and how evolution affects the dynamics of the competing species-the key step for completing the required eco-evolutionary feedback-has been difficult to resolve. Here, we show that evolution in response to interspecific competition feeds back to change the course of competitive population dynamics of aquatic plant species over 10-15 generations in the field. By manipulating selection imposed by heterospecific competitors in experimental ponds, we demonstrate that (i) interspecific competition drives rapid genotypic change, and (ii) this evolutionary change in one competitor, while not changing the coexistence outcome, causes the population trajectories of the two competing species to converge. In contrast to the common expectation that interspecific competition should drive the evolution of niche differentiation, our results suggest that genotypic evolution resulted in phenotypic changes that altered population dynamics by affecting the competitive hierarchy. This result is consistent with theory suggesting that competition for essential resources can limit opportunities for the evolution of niche differentiation. Our finding that rapid evolution regulates the dynamics of competing species suggests that ecosystems may rely on continuous feedbacks between ecology and evolution to maintain species diversity.

Demographic responses underlying eco-evolutionary dynamics as revealed with inverse modelling.

Changes in population dynamics due to interacting evolutionary and ecological processes are the direct result of responses in vital rates, that is stage-specific growth, survival and fecundity. Quantifying through which vital rates population fitness is affected, instead of focusing on population trends only, can give a more mechanistic understanding of eco-evolutionary dynamics. The aim of this study was to estimate the underlying demographic rates of aphid (Myzus persicae) populations. We analysed unpublished stage-structure population dynamics data of a field experiment with caged and uncaged populations in which rapid evolutionary dynamics were observed, as well as unpublished results from an individual life table experiment performed in a glasshouse. Using data on changes in population abundance and stage distributions over time, we estimated transition matrices with inverse modelling techniques, in a Bayesian framework. The model used to fit across all experimental treatments included density as well as clone-specific caging effects. We additionally used individual life table data to inform the model on survival, growth and reproduction. Results suggest that clones varied considerably in vital rates, and imply trade-offs between reproduction and survival. Responses to densities also varied between clones. Negative density dependence was found in growth and reproduction, and the presence of predators and competitors further decreased these two vital rates, while survival estimates increased. Under uncaged conditions, population growth rates of the evolving populations were increased compared to the expectation based on the pure clones. Our inverse modelling approach revealed how much vital rates contributed to the eco-evolutionary dynamics. The decomposition analysis showed that variation in population growth rates in the evolving populations was to a large extent shaped by plant size. Yet, it also revealed an impact of evolutionary changes in clonal composition. Finally, we discuss that inverse modelling is a complex problem, as multiple combinations of individual rates can result in the same dynamics. We discuss assumptions and limitations, as well as opportunities, of this approach.

Plant domestication slows pest evolution.

Agricultural practices such as breeding resistant varieties and pesticide use can cause rapid evolution of pest species, but it remains unknown how plant domestication itself impacts pest contemporary evolution. Using experimental evolution on a comparative phylogenetic scale, we compared the evolutionary dynamics of a globally important economic pest - the green peach aphid (Myzus persicae) - growing on 34 plant taxa, represented by 17 crop species and their wild relatives. Domestication slowed aphid evolution by 13.5%, maintained 10.4% greater aphid genotypic diversity and 5.6% higher genotypic richness. The direction of evolution (i.e. which genotypes increased in frequency) differed among independent domestication events but was correlated with specific plant traits. Individual-based simulation models suggested that domestication affects aphid evolution directly by reducing the strength of selection and indirectly by increasing aphid density and thus weakening genetic drift. Our results suggest that phenotypic changes during domestication can alter pest evolutionary dynamics.

Adaptive evolution in ecological communities.

Understanding how natural selection drives evolution is a key challenge in evolutionary biology. Most studies of adaptation focus on how a single environmental factor, such as increased temperature, affects evolution within a single species. The biological relevance of these experiments is limited because nature is infinitely more complex. Most species are embedded within communities containing many species that interact with one another and the physical environment. To understand the evolutionary significance of such ecological complexity, experiments must test the evolutionary impact of interactions among multiple species during adaptation. Here we highlight an experiment that manipulates species composition and tracks evolutionary responses within each species, while testing for the mechanisms by which species interact and adapt to their environment. We also discuss limitations of previous studies of adaptive evolution and emphasize how an experimental evolution approach can circumvent such shortcomings. Understanding how community composition acts as a selective force will improve our ability to predict how species adapt to natural and human-induced environmental change.

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants.

The consumption of plants by animals underlies important evolutionary and ecological processes in nature. Arthropod herbivory evolved approximately 415 Ma and the ensuing coevolution between plants and herbivores is credited with generating much of the macroscopic diversity on the Earth. In contemporary ecosystems, herbivory provides the major conduit of energy from primary producers to consumers. Here, we show that when averaged across all major lineages of vascular plants, herbivores consume 5.3% of the leaf tissue produced annually by plants, whereas previous estimates are up to 3.8× higher. This result suggests that for many plant species, leaf herbivory may play a smaller role in energy and nutrient flow than currently thought. Comparative analyses of a diverse global sample of 1058 species across 2085 populations reveal that models of stabilizing selection best describe rates of leaf consumption, and that rates vary substantially within and among major plant lineages. A key determinant of this variation is plant growth form, where woody plant species experience 64% higher leaf herbivory than non-woody plants. Higher leaf herbivory in woody species supports a key prediction of the plant apparency theory. Our study provides insight into how a long history of coevolution has shaped the ecological and evolutionary relationships between plants and herbivores.

The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events.

The domestication of crops is among the most important innovations in human history. Here, we test the hypothesis that cultivation and artificial selection for increased productivity of crops reduced plant defenses against herbivores. We compared the performance of two economically important generalist herbivores - the leaf-chewing beet armyworm (Spodoptera exigua) and the phloem-feeding green peach aphid (Myzus persicae) - across 29 crop species and their closely related wild relatives. We also measured putative morphological and chemical defensive traits and correlated them with herbivore performance. We show that, on average, domestication significantly reduced resistance to S. exigua, but not M. persicae, and that most independent domestication events did not cause differences in resistance to either herbivore. In addition, we found that multiple plant traits predicted resistance to S. exigua and M. persicae, and that domestication frequently altered the strength and direction of correlations between these traits and herbivore performance. Our results show that domestication can alter plant defenses, but does not cause strong allocation tradeoffs as predicted by plant defense theory. These results have important implications for understanding the evolutionary ecology of species interactions and for the search for potential resistance traits to be targeted in crop breeding.

Two duckweed species exhibit variable tolerance to microcystin-LR exposure across genotypic lineages.

Cyanotoxins produced by harmful cyanobacteria blooms can damage freshwater ecosystems and threaten human health. Floating macrophytes may be used as a means of biocontrol by limiting light and resources available to cyanobacteria. However, genetic variation in macrophyte sensitivity to cyanotoxins could influence their suitability as biocontrol agents. We investigated the influence of such intraspecific variation on the response of two rapidly growing duckweed species, Lemna minor and Spirodela polyrhiza, often used in nutrient and metal bioremediation. We assessed two biomarkers related to productivity (biomass and chlorophyll A production) and two related to fitness measures (population size and growth rate). Fifteen genetic lineages of each species were grown in media containing common cyanotoxin microcystin-LR at ecologically relevant concentrations or control media for a period of twelve days. Genotype identity had a strong impact on all biomarker responses. Microcystin concentration slightly increased the final population sizes of both macrophyte species with a marginal effect on growth rate of L. minor and the chlorophyll A production of S. polyrhiza, but overall these species were very tolerant of microcystin. The strong tolerance supports the potential use of these plants as bioremediators of cyanobacterial blooms. However, differential impact of microcystin exposure discovered in single lineage models among genotypes indicates a potential for cyanotoxins to act as selective forces, necessitating attention to genotype selection for bioremediation.

Neopolyploidy increases stress tolerance and reduces fitness plasticity across multiple urban pollutants: support for the "general-purpose" genotype hypothesis.

Whole-genome duplication is a common macromutation with extensive impacts on gene expression, cellular function, and whole-organism phenotype. As a result, it has been proposed that polyploids have "general-purpose" genotypes that perform better than their diploid progenitors under stressful conditions. Here, we test this hypothesis in the context of stresses presented by anthropogenic pollutants. Specifically, we tested how multiple neotetraploid genetic lineages of the mostly asexually reproducing greater duckweed (Spirodela polyrhiza) perform across a favorable control environment and 5 urban pollutants (iron, salt, manganese, copper, and aluminum). By quantifying the population growth rate of asexually reproducing duckweed over multiple generations, we found that across most pollutants, but not all, polyploidy decreased the growth rate of actively growing propagules but increased that of dormant ones. Yet, when considering total propagule production, polyploidy increased tolerance to most pollutants, and polyploids maintained population-level fitness across pollutants better than diploids. Furthermore, broad-sense genetic correlations in growth rate among pollutants were all positive in neopolyploids but not so for diploids. Our results provide a rare test and support for the hypothesis that polyploids are more tolerant of stressful conditions and can maintain fitness better than diploids across heterogeneous stresses. These results may help predict that polyploids may be likely to persist in stressful environments, such as those caused by urbanization and other human activities.

Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid.

An eco-evolutionary feedback loop is defined as the reciprocal impacts of ecology on evolutionary dynamics and evolution on ecological dynamics on contemporary timescales. We experimentally tested for an eco-evolutionary feedback loop in the green peach aphid, Myzus persicae, by manipulating initial densities and evolution. We found strong evidence that initial aphid density alters the rate and direction of evolution, as measured by changes in genotype frequencies through time. We also found that evolution of aphids within only 16 days, or approximately three generations, alters the rate of population growth and predicts density compared to nonevolving controls. The impact of evolution on population dynamics also depended on density. In one evolution treatment, evolution accelerated population growth by up to 10.3% at high initial density or reduced it by up to 6.4% at low initial density. The impact of evolution on population growth was as strong as or stronger than that caused by a threefold change in intraspecific density. We found that, taken together, ecological condition, here intraspecific density, alters evolutionary dynamics, which in turn alter concurrent population growth rate (ecological dynamics) in an eco-evolutionary feedback loop. Our results suggest that ignoring evolution in studies predicting population dynamics might lead us to over- or underestimate population density and that we cannot predict the evolutionary outcome within aphid populations without considering population size.

Phenotypic plasticity promotes species coexistence.

Ecological explanations for species coexistence assume that species' traits, and therefore the differences between species, are fixed on short timescales. However, species' traits are not fixed, but can instead change rapidly as a consequence of phenotypic plasticity. Here we use a combined experimental-theoretical approach to demonstrate that plasticity in response to interspecific competition between two aquatic plants allows for species coexistence where competitive exclusion is otherwise predicted to occur. Our results show that rapid trait changes in response to a shift in the competitive environment can promote coexistence in a way that is not captured by common measures of niche differentiation.

The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics.

Rapid evolution challenges the assumption that evolution is too slow to impact short-term ecological dynamics. This insight motivates the study of 'Eco-Evolutionary Dynamics' or how evolution and ecological processes reciprocally interact on short time scales. We tested how rapid evolution impacts concurrent population dynamics using an aphid (Myzus persicae) and an undomesticated host (Hirschfeldia incana) in replicated wild populations. We manipulated evolvability by creating non-evolving (single clone) and potentially evolving (two-clone) aphid populations that contained genetic variation in intrinsic growth rate. We observed significant evolution in two-clone populations whether or not they were exposed to predators and competitors. Evolving populations grew up to 42% faster and attained up to 67% higher density, compared with non-evolving control populations but only in treatments exposed to competitors and predators. Increased density also correlates with relative fitness of competing clones suggesting a full eco-evolutionary dynamic cycle defined as reciprocal interactions between evolution and density.

Eco-evolutionary interaction between microbiome presence and rapid biofilm evolution determines plant host fitness.

Microbiomes are important to the survival and reproduction of their hosts. Although ecological and evolutionary processes can happen simultaneously in microbiomes, little is known about how microbiome eco-evolutionary dynamics determine host fitness. Here we show, using experimental evolution, that fitness of the aquatic plant Lemna minor is modified by interactions between the microbiome and the evolution of one member, Pseudomonas fluorescens. Microbiome presence promotes P. fluorescens' rapid evolution to form biofilm, which reciprocally alters the microbiome's species composition. These eco-evolutionary dynamics modify the host's multigenerational fitness. The microbiome and non-evolving P. fluorescens together promote host fitness, whereas the microbiome with P. fluorescens that evolves biofilm reduces the beneficial impact on host fitness. Additional experiments suggest that the microbial effect on host fitness may occur through changes in microbiome production of auxin, a plant growth hormone. Our study, therefore, experimentally demonstrates the importance of the eco-evolutionary dynamics in microbiomes for host-microbiome interactions.

Damage and recovery from drift of synthetic-auxin herbicide dicamba depends on concentration and varies among floral, vegetative, and lifetime traits in rapid cycling Brassica rapa.

Herbicides can drift from intended plants onto non-target species. It remains unclear how drift impacts plant functional traits that are important for fitness. To address this gap, we conducted an experiment where fast cycling Brassica rapa plants were exposed to one of three drift concentrations (0.5%, 1%, 10%) of synthetic-auxin dicamba. We evaluated damage to and capacity of floral and vegetative traits to recover as well as lifetime fitness by comparing treated plants to controls. Response to dicamba exposure was concentration-dependent across all traits but varied with trait type. At 0.5% dicamba, three out of five floral traits were affected, while at 1% dicamba, four floral traits and one out of two vegetative traits were negatively impacted. At 10% dicamba all floral and vegetative traits were stunted. Overall, floral traits were more responsive to all dicamba drift concentrations than vegetative traits and displayed a wide range of variation ranging from no response (e.g., pistil length) to up to 84% reduction (ovule number). However, despite floral traits were more affected across the dicamba drift concentrations they were also more likely to recover than the vegetative traits. There was also variation among lifetime traits; the onset of flowering was delayed, and reproductive fitness was negatively affected in a concentration-dependent manner, but the final biomass and total flower production were not affected. Altogether, we show substantial variation across plant traits in their response to dicamba and conclude that accounting for this variation is essential to understand the full impact of herbicide drift on plants and the ecological interactions these traits mediate.

On the Origin of Coexisting Species.

Speciation is frequently initiated but rarely completed, a phenomenon hypothesized to arise due to the failure of nascent lineages to persist. Although a failure to persist often has ecological causes, key gaps exist between ecological and evolutionary theories that, if filled, would clarify when and why speciation succeeds or fails. Here, we apply ecological coexistence theory to show how the alignment between different forms of niche opportunity and niche use shape the initiation, progression, and completion of speciation. Niche evolution may drive coexistence or competitive exclusion, and an ability to coexist ecologically may help or hinder speciation. Our perspective allows progress towards unifying the origin and maintenance of species diversity across the tree of life.

Environmental factors influencing adult sex ratio in Trinidadian guppies.

Sex ratios can influence mating behaviour, population dynamics and evolutionary trajectories; yet the causes of natural sex ratio variation are often uncertain. Although secondary (birth) sex ratios in guppies (Poecilia reticulata) are typically 1:1, we recorded female-biased tertiary (adult) sex ratios in about half of our 48 samples and male-biased sex ratios in none of them. This pattern implies that some populations experience male-biased mortality, perhaps owing to variation in predation or resource limitation. We assessed the effects of predation and/or inter-specific resource competition (intraguild predation) by measuring the local catch-per-unit-effort (CPUE) of species (Rivulus killifish and Macrobrachium prawns) that may differentially prey on male guppies. We assessed the effects of resource levels by measuring canopy openness and algal biomass (chlorophyll a concentration). We found that guppy sex ratios were increasingly female-biased with increasing CPUE of Macrobrachium, and perhaps also Rivulus, and with decreasing canopy openness. We also found an interaction between predators and resource levels in that the effect of canopy openness was greatest when Macrobrachium CPUE was highest. Our study thus also reveals the value of simultaneously testing multiple environmental factors that may drive tertiary sex ratio variation.

What genomic data can reveal about eco-evolutionary dynamics.

Recognition that evolution operates on the same timescale as ecological processes has motivated growing interest in eco-evolutionary dynamics. Nonetheless, generating sufficient data to test predictions about eco-evolutionary dynamics has proved challenging, particularly in natural contexts. Here we argue that genomic data can be integrated into the study of eco-evolutionary dynamics in ways that deepen our understanding of the interplay between ecology and evolution. Specifically, we outline five major questions in the study of eco-evolutionary dynamics for which genomic data may provide answers. Although genomic data alone will not be sufficient to resolve these challenges, integrating genomic data can provide a more mechanistic understanding of the causes of phenotypic change, help elucidate the mechanisms driving eco-evolutionary dynamics, and lead to more accurate evolutionary predictions of eco-evolutionary dynamics in nature.