Microbial responses to stress cryptically alter natural selection on plants.

Microbial communities can rapidly respond to stress, meaning plants may encounter altered soil microbial communities in stressful environments. These altered microbial communities may then affect natural selection on plants. Because stress can cause lasting changes to microbial communities, microbes may also cause legacy effects on plant selection that persist even after the stress ceases. To explore how microbial responses to stress and persistent microbial legacy effects of stress affect natural selection, we grew Chamaecrista fasciculata plants in stressful (salt, herbicide, or herbivory) or nonstressful conditions with microbes that had experienced each of these environments in the previous generation. Microbial community responses to stress generally counteracted the effects of stress itself on plant selection, thereby weakening the strength of stress as a selective agent. Microbial legacy effects of stress altered plant selection in nonstressful environments, suggesting that stress-induced changes to microbes may continue to affect selection after stress is lifted. These results suggest that soil microbes may play a cryptic role in plant adaptation to stress, potentially reducing the strength of stress as a selective agent and altering the evolutionary trajectory of plant populations.

What Can Evolutionary History Tell Us about the Functioning of Ecological Communities? The ASN Presidential Debate.

AbstractIn January 2018, Sharon Strauss, then president of the American Society of Naturalists, organized a debate on the following topic: does evolutionary history inform the current functioning of ecological communities? The debaters-Ives, Lau, Mayfield, and Tobias-presented pro and con arguments, caricatured in standard debating format. Numerous examples show that both recent microevolutionary and longer-term macroevolutionary history are important to the ecological functioning of communities. On the other hand, many other examples illustrate that the evolutionary history of communities or community members does not influence ecological function, or at least not very much. This article aims to provide a provocative discussion of the consistent and conflicting patterns that emerge in the study of contemporary and historical evolutionary influences on community function, as well as to identify questions for further study. It is intended as a thought-provoking exercise to explore this complex field, specifically addressing (1) key assumptions and how they can lead us astray and (2) issues that need additional study. The debaters all agree that evolutionary history can inform us about at least some aspects of community function. The underlying question at the root of the debate, however, is how the fields of ecology and evolution can most profitably collaborate to provide a deeper and broader understanding of ecological communities.

How ecological and evolutionary theory expanded the 'ideal weed' concept.

Since Baker's attempt to characterize the 'ideal weed' over 50 years ago, ecologists have sought to identify features of species that predict invasiveness. Several of Baker's 'ideal weed' traits are well studied, and we now understand that many traits can facilitate different components of the invasion process, such as dispersal traits promoting transport or selfing enabling establishment. However, the effects of traits on invasion are context dependent. The traits promoting invasion in one community or at one invasion stage may inhibit invasion of other communities or success at other invasion stages, and the benefits of any given trait may depend on the other traits possessed by the species. Furthermore, variation in traits among populations or species is the result of evolution. Accordingly, evolution both prior to and after invasion may determine invasion outcomes. Here, we review how our understanding of the ecology and evolution of traits in invasive plants has developed since Baker's original efforts, resulting from empirical studies and the emergence of new frameworks and ideas such as community assembly theory, functional ecology, and rapid adaptation. Looking forward, we consider how trait-based approaches might inform our understanding of less-explored aspects of invasion biology ranging from invasive species responses to climate change to coevolution of invaded communities.

Traits of soil bacteria predict plant responses to soil moisture.

Microorganisms can help plants and animals contend with abiotic stressors, but why they provide such benefits remains unclear. Here we investigated byproduct benefits, which occur when traits that increase the fitness of one species provide incidental benefits to another species with no direct cost to the provider. In a greenhouse experiment, microbial traits predicted plant responses to soil moisture such that bacteria with self-beneficial traits in drought increased plant early growth, size at reproduction, and chlorophyll concentration under drought, while bacteria with self-beneficial traits in well-watered environments increased these same plant traits in well-watered soils. Thus, microbial traits that promote microbial success in different moisture environments also promote plant success in these same environments. Our results demonstrate that byproduct benefits, a concept developed to explain the evolution of cooperation in pairwise mutualisms, can also extend to interactions between plants and nonsymbiotic soil microbes.

Mutualisms in a warming world: How increased temperatures affect the outcomes of multi-mutualist interactions.

In nature, plant species simultaneously interact with many different mutualistic partners. These mutualists may influence one another through direct interference or indirectly by competing for shared reward resources or through alteration of plant traits. Together, these mutualists also may combine to affect plant hosts in ways that may not be predictable based on pairwise interactions. Given that the outcome of mutualistic interactions often depends on environmental conditions, multi-mutualist effects on one another, and their plant hosts may be affected by global changes. Here, we grew focal plants under simulated global warming conditions and manipulated the presence of partner mutualists to test how warming affects the outcome of interactions between focal plants and their partners (nitrogen-fixing rhizobia, ant defenders, and pollinators) and interactions among these partner mutualists. We find that warming alters the fitness benefits plants receive from rhizobium resource mutualists but not ant mutualists and that warming altered plant investment in all mutualists. We also find that mutualist partners interact, often by altering the availability of plant-produced rewards that facilitate interactions with other partners. Our work illustrates that global changes may affect some but not all mutualisms, often asymmetrically (e.g., affecting investment in the mutualist partner but not plant host benefits) and also highlights the ubiquity of interactions between the multiple mutualists associating with a shared host.

Evolutionary effects of nitrogen are not easily predicted from ecological responses.

PREMISE: Anthropogenic nitrogen (N) addition alters the abiotic and biotic environment, potentially leading to changes in patterns of natural selection (i.e., trait-fitness relationships) and the opportunity for selection (i.e., variance in relative fitness). Because N addition favors species with light acquisition strategies (e.g., tall species), we predicted that N would strengthen selection favoring those same traits. We also predicted that N could alter the opportunity for selection via its effects on mean fitness and/or competitive asymmetries. METHODS: We quantified the strength of selection and the opportunity for selection in replicated populations of the annual grass Setaria faberi (giant foxtail) growing in a long-term N addition experiment. We also correlated these population-level parameters with community-level metrics to identify the proximate causes of N-mediated evolutionary effects. RESULTS: N addition increased aboveground productivity, light asymmetry, and reduced species diversity. Contrary to expectations, N addition did not strengthen selection for trait values associated with higher light acquisition such as greater height and specific leaf area (SLA); rather, it strengthened selection favoring lower SLA. Light asymmetry and species diversity were associated with selection for height and SLA, suggesting a role for these factors in driving N-mediated selection. The opportunity for selection was not influenced by N addition but was negatively associated with species diversity. CONCLUSIONS: Our results indicate that anthropogenic N enrichment can affect evolutionary processes, but that evolutionary changes in plant traits within populations are unlikely to parallel the shifts in plant traits observed at the community level.

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.

Linking genetic diversity and species diversity through plant-soil feedback.

Genetic diversity and species diversity are typically studied in isolation despite theory showing they likely influence one another. Here, we used simplified communities of one or two populations of one or two species to test whether linkages between genetic and species diversity can be mediated by interactions between plants and their soil microbiota, or microbe-mediated plant-soil feedback (PSF). Interspecific PSF promotes the maintenance of species diversity when plants grow better with heterospecific soil microbes than with conspecific microbes. Similarly, intraspecific PSF promotes the maintenance of genetic diversity when plants grow better with heterogenotypic than with congenotypic microbes. In a two-phase greenhouse experiment, we conditioned the soil microbial community with pairs of plants that were either two individuals of the same species (lower species diversity) or one individual of each of two species (higher species diversity), and with pairs of plants that were either two individuals from the same population (lower genetic diversity) or one individual from each of two populations (higher genetic diversity). We then tested the effects of these microbial communities on plant growth in a second phase. We found that higher genetic diversity reduced the ability of interspecific PSF to promote plant species diversity, and for one of our two study species, higher species diversity reduced the ability of intraspecific PSF to promote plant genetic diversity. If these patterns occur in more diverse communities, then our results suggest that PSF may dampen the negative effects of diversity loss by promoting diversity at other levels of biological organization.

Plant-microbe eco-evolutionary dynamics in a changing world.

Both plants and their associated microbiomes can respond strongly to anthropogenic environmental changes. These responses can be both ecological (e.g. a global change affecting plant demography or microbial community composition) and evolutionary (e.g. a global change altering natural selection on plant or microbial populations). As a result, global changes can catalyse eco-evolutionary feedbacks. Here, we take a plant-focused perspective to discuss how microbes mediate plant ecological responses to global change and how these ecological effects can influence plant evolutionary response to global change. We argue that the strong and functionally important relationships between plants and their associated microbes are particularly likely to result in eco-evolutionary feedbacks when perturbed by global changes and discuss how improved understanding of plant-microbe eco-evolutionary dynamics could inform conservation or even agriculture.

Do southern seed or soil microbes mitigate the effects of warming on establishing prairie plant communities?

Restoration in this era of climate change comes with a new challenge: anticipating how best to restore populations to persist under future climate conditions. Specifically, it remains unknown whether locally adapted or warm-adapted seeds best promote native plant community restoration in the warmer conditions predicted in the future and whether local or warm-adapted soil microbial communities could mitigate plant responses to warming. This may be especially relevant for biomes spanning large climatic gradients, such as the North American tallgrass prairie. Here, we used a short-term mesocosm experiment to evaluate how seed provenances (Local Northern region, Non-local Northern region, Non-local Southern region) of 10 native tallgrass prairie plants (four forbs, two legumes, and four grasses) responded to warmer conditions predicted in the future and how soil microbial communities from those three regions influenced these responses. Warming and seed provenance affected plant community composition and warming decreased plant diversity for all three seed provenances. Plant species varied in their individual responses to warming, and across species, we detected no consistent differences among the three provenances in terms of biomass response to warming and few strong effects of soil provenance. Our work provides evidence that warming, in part, may reduce plant diversity and affect restored prairie composition. Because the southern provenance did not consistently outperform others under warming and we found little support for the "local is best" paradigm currently dominating restoration practice, identifying appropriate seed provenances to promote restoration success both now and in future warmer environments may be challenging. Due to the idiosyncratic responses across species, we recommend that land managers compare seeds from different regions for each species to determine which seed provenance performs best under warming and in restoration for tallgrass prairies.

Extirpated prairie species demonstrate more variable phenological responses to warming than extant congeners.

PREMISE: Shifting phenology in response to climate is one mechanism that can promote population persistence and geographic spread; therefore, species with limited ability to phenologically track changing environmental conditions may be more susceptible to population declines. Alternatively, apparently nonresponding species may demonstrate divergent responses to multiple environmental conditions experienced across seasons. METHODS: Capitalizing on herbarium records from across the midwestern United States and on detailed botanical surveys documenting local extinctions over the past century, we investigated whether extirpated and extant taxa differ in their phenological responses to temperature and precipitation during winter and spring (during flowering and the growing season before flowering) or in the magnitude of their flowering time shift over the past century. RESULTS: Although warmer temperatures across seasons advanced flowering, extirpated and extant species differed in the magnitude of their phenological responses to winter and spring warming. Extirpated species demonstrated inconsistent phenological responses to warmer spring temperatures, whereas extant species consistently advanced flowering in response to warmer spring temperatures. In contrast, extirpated species advanced flowering more than extant species in response to warmer winter temperatures. Greater spring precipitation tended to delay flowering for both extirpated and extant taxa. Finally, both extirpated and extant taxa delayed flowering over time. CONCLUSIONS: This study highlights the importance of understanding phenological responses to seasonal warming and indicates that extirpated species may demonstrate more variable phenological responses to temperature than extant congeners, a finding consistent with the hypothesis that appropriate phenological responses may reduce species' likelihood of extinction.

Microbe-mediated adaptation in plants.

Interactions with microbial symbionts have yielded great macroevolutionary innovations across the tree of life, like the origins of chloroplasts and the mitochondrial powerhouses of eukaryotic cells. There is also increasing evidence that host-associated microbiomes influence patterns of microevolutionary adaptation in plants and animals. Here we describe how microbes can facilitate adaptation in plants and how to test for and differentiate between the two main mechanisms by which microbes can produce adaptive responses in higher organisms: microbe-mediated local adaptation and microbe-mediated adaptive plasticity. Microbe-mediated local adaptation is when local plant genotypes have higher fitness than foreign genotypes because of a genotype-specific affiliation with locally beneficial microbes. Microbe-mediated adaptive plasticity occurs when local plant phenotypes, elicited by either the microbial community or the non-microbial environment, have higher fitness than foreign phenotypes as a result of interactions with locally beneficial microbes. These microbial effects on adaptation can be difficult to differentiate from traditional modes of adaptation but may be prevalent. Ignoring microbial effects may lead to erroneous conclusions about the traits and mechanisms underlying adaptation, hindering management decisions in conservation, restoration, and agriculture.

Symbiosis and stress: how plant microbiomes affect host evolution.

Existing paradigms for plant microevolution rarely acknowledge the potential impacts of diverse microbiomes on evolutionary processes. Many plant-associated microorganisms benefit the host via access to resources, protection from pathogens, or amelioration of abiotic stress. In doing so, they alter the plant's perception of the environment, potentially reducing the strength of selection acting on plant stress tolerance or defence traits or altering the traits that are the target of selection. We posit that the microbiome can affect plant microevolution via (1) manipulation of plant phenotypes in ways that increase plant fitness under stress and (2) direct microbial responses to the environment that benefit the plant. Both mechanisms might favour plant genotypes that attract or stimulate growth of the most responsive microbial populations or communities. We provide support for these scenarios using infectious disease and quantitative genetics models. Finally, we discuss how beneficial plant-microbiome associations can evolve if traditional mechanisms maintaining cooperation in pairwise symbioses, namely partner fidelity, partner choice and fitness alignment, also apply to the interactions between plants and diverse foliar and soil microbiomes. To understand the role of the plant microbiome in host evolution will require a broad ecological understanding of plant-microbe interactions across both space and time. This article is part of the theme issue 'The role of the microbiome in host evolution'.

Evolution in novel environments: Do restored prairie populations experience strong selection?

When populations colonize new habitats, they are likely to experience novel environmental conditions, and as a consequence may experience strong selection. While selection and the resulting evolutionary responses may have important implications for establishment success in colonizing populations, few studies have estimated selection in such scenarios. Here we examined evidence of selection in recently established plant populations in two prairie restorations in close proximity (<15 km apart) using two approaches: (1) we tested for evidence of past selection on a suite of traits in two Chamaecrista fasciculata populations by comparing the restored populations to each other and their shared source population in common gardens to quantify evolutionary responses and (2) we measured selection in the field. We found evidence of past selection on flowering time, specific leaf area, and root nodule production in one of the populations, but detected contemporary selection on only one trait (plant height). Our findings demonstrate that while selection can occur in colonizing populations, resulting in significant trait differences between restored populations in fewer than six generations, evolutionary responses differ across even nearby populations sown with the same source population. Because contemporary measures of selection differed from evolutionary responses to past selection, our findings also suggest that selection likely differs over the early stages of succession that characterize young prairies.

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.

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.

Phenology in a warming world: differences between native and non-native plant species.

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non-native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non-native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non-native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non-native species, implicating phenology as a potential trait associated with the successful establishment of non-native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non-natives are hypothesised to promote invasion success and population persistence, potentially benefiting non-native over native species under climate change.

Species characteristics affect local extinctions.

PREMISE OF THE STUDY: Human activities threaten thousands of species with extinction. However, it remains difficult to predict extinction risk for many vulnerable species. Species traits, species characteristics such as rarity or habitat use, and phylogenetic patterns are associated with responses to anthropogenic environmental change and may help predict likelihood of extinction. METHODS: We used historical botanical data from Kalamazoo County, Michigan, USA, to examine whether species traits (growth form, life history, nitrogen-fixation, photosynthetic pathway), species characteristics (community association, species origin, range edge, habitat specialization, rarity), or phylogenetic relatedness explain local species loss at the county level. KEY RESULTS: Across Kalamazoo County, prairie species, species at the edge of their native range, regionally rare species, and habitat specialists were most likely to become locally extinct. Prairie species experienced the highest local extinction rates of any habitat type, and among prairie species, regionally rare and specialist species were most vulnerable to loss. We found no evidence for a phylogenetic pattern in plant extinctions. CONCLUSIONS: Our study illustrates the value of historical datasets for understanding and potentially predicting biodiversity loss. Not surprisingly, rare, specialist species occupying threatened habitats are most at risk of local extinction. As a result, identifying mechanisms to conserve or restore rare or declining species and preventing further habitat destruction may be the most effective strategies for reducing future extinction.

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.