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.

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.

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.

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.

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.

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.

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.

Effects of multiple mutualists on plants and their associated arthropod communities.

Although most studies of mutualisms focus on a single partner at a time, host species often associate with multiple mutualist partners simultaneously. Because of potential interactions between mutualists, only studying a single type of mutualism could lead to a biased perspective of mutualism benefit and how mutualisms may scale-up to affect communities. The legume Chamaecrista fasciculata engages in a resource mutualism with nitrogen-fixing rhizobia and also forms symbiotic interactions with ants by providing nectar in exchange for defense against herbivores. Although they provide very different benefits to the plant, both mutualists receive carbon resources from the plant. As a result, these two mutualists are likely to interact, potentially competing for carbon resources or mutually benefitting each other via their positive effects on plant hosts. In a full-factorial field experiment, we explored how rhizobia and ants influence one another, C. fasciculata fitness, and the associated arthropod community. Ants reduced plant allocation to rhizobia, but ants also increased rhizobia contamination of uninoculated plants, suggesting that ants may disperse rhizobia. In turn, rhizobia increased ant abundances, with ants preferentially tending plants with rhizobia. Chamaecrista fasciculata received substantial fitness benefits from rhizobia; in contrast, associating with ants reduced fitness. Additionally, the mutualists interacted to influence the abundance of other arthropods found on the plants. Rhizobia increased arthropod abundances, likely because more nitrogen-rich leaf tissue was more attractive to arthropod herbivores, but ants negated these increases. As these results illustrate, multiple mutualists may interact, influencing each other's abundance and the abundance of other community members.

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.

Long-Term Research in Ecology and Evolution (LTREE): 2015 survey data.

To systematically assess views on contributions and future activities for long-term research in ecology and evolution (LTREE), we conducted and here provide data responses and associated metadata for a survey of ecological and evolutionary scientists. The survey objectives were to: (1) Identify and prioritize research questions that are important to address through long-term, ecological field experiments; and (2) understand the role that these experiments might play in generating and applying ecological and evolutionary knowledge. The survey was developed adhering to the standards of the American Association for Public Opinion Research. It was administered online using Qualtrics Survey Software. Survey creation was a multi-step process, with questions and format developed and then revised with, for example, input from an external advisory committee comprising senior and junior ecological and evolutionary researchers. The final questionnaire was released to ~100 colleagues to ensure functionality and then fielded 2 d later (January 7th , 2015). Two professional societies distributed it to their membership, including the Ecological Society of America, and it was posted to three list serves. The questionnaire was available through February 8th 2015 and completed by 1,179 respondents. The distribution approach targeted practicing ecologists and evolutionary biologists in the U.S. Quantitative (both ordinal and categorical) closed-ended questions used a predefined set of response categories, facilitating direct comparison across all respondents. Qualitative, open-ended questions, provided respondents the opportunity to develop their own answers. We employed quantitative questions to score views on the extent to which long-term experimental research has contributed to understanding in ecology and evolutionary biology; its role compared to other approaches (e.g., short-term experiments); justifications for and caveats to long-term experiments; and the relative importance of incentives for conducting long-term research. Qualitative questions were used to assess community views on the most important topics and questions for long-term research to address, and primary incentives and challenges to realizing this work. Finally, demographic data were collected to determine if views were conditional on such things as years of experience and field of expertise. The final questionnaire and all responses are provided for unrestricted use.

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.

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.

Ecological genomics of mutualism decline in nitrogen-fixing bacteria.

Anthropogenic changes can influence mutualism evolution; however, the genomic regions underpinning mutualism that are most affected by environmental change are generally unknown, even in well-studied model mutualisms like the interaction between legumes and their nitrogen (N)-fixing rhizobia. Such genomic information can shed light on the agents and targets of selection maintaining cooperation in nature. We recently demonstrated that N-fertilization has caused an evolutionary decline in mutualistic partner quality in the rhizobia that form symbiosis with clover. Here, population genomic analyses of N-fertilized versus control rhizobium populations indicate that evolutionary differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) contributes to partner quality decline. Moreover, patterns of genetic variation at selected loci were consistent with recent positive selection within N-fertilized environments, suggesting that N-rich environments might select for less beneficial rhizobia. By studying the molecular population genomics of a natural bacterial population within a long-term ecological field experiment, we find that: (i) the N environment is indeed a potent selective force mediating mutualism evolution in this symbiosis, (ii) natural variation in rhizobium partner quality is mediated in part by key symbiosis genes on the symbiotic plasmid, and (iii) differentiation at selected genes occurred in the context of otherwise recombining genomes, resembling eukaryotic models of adaptation.