Prairie restoration promotes the abundance and diversity of mutualistic arbuscular mycorrhizal fungi.

Predicting how biological communities assemble in restored ecosystems can assist in conservation efforts, but most research has focused on plants, with relatively little attention paid to soil microbial organisms that plants interact with. Arbuscular mycorrhizal (AM) fungi are an ecologically significant functional group of soil microbes that form mutualistic symbioses with plants and could therefore respond positively to plant community restoration. To evaluate the effects of plant community restoration on AM fungi, we compared AM fungal abundance, species richness, and community composition of five annually cultivated, conventionally managed agricultural fields with paired adjacent retired agricultural fields that had undergone prairie restoration 5-9 years prior to sampling. We hypothesized that restoration stimulates AM fungal abundance and species richness, particularly for disturbance-sensitive taxa, and that gains of new taxa would not displace AM fungal species present prior to restoration due to legacy effects. AM fungal abundance was quantified by measuring soil spore density and root colonization. AM fungal species richness and community composition were determined in soils and plant roots using DNA high-throughput sequencing. Soil spore density was 2.3 times higher in restored prairies compared to agricultural fields, but AM fungal root colonization did not differ between land use types. AM fungal species richness was 2.7 and 1.4 times higher in restored prairies versus agricultural fields for soil and roots, respectively. The abundance of Glomeraceae, a disturbance-tolerant family, decreased by 25% from agricultural to restored prairie soils but did not differ in plant roots. The abundance of Claroideoglomeraceae and Diversisporaceae, both disturbance-sensitive families, was 4.6 and 3.2 times higher in restored prairie versus agricultural soils, respectively. Species turnover was higher than expected relative to a null model, indicating that AM fungal species were gained by replacement. Our findings demonstrate that restoration can promote a relatively rapid increase in the abundance and diversity of soil microbial communities that had been degraded by decades of intensive land use, and community compositional change can be predicted by the disturbance tolerance of soil microbial taxonomic and functional groups.

The welfare problems of wide-ranging Carnivora reflect naturally itinerant lifestyles.

Carnivora with naturally small home ranges readily adjust to the evolutionarily new environment of captivity, but wider-ranging species seem prone to stress. Understanding why would advance both collection planning and enclosure design. We therefore investigated which aspects of wide-ranging lifestyles are key. We identified eight correlates of home range size (reflecting energetic needs, movement, intra-specific interactions, and itinerant lifestyles). We systematically assessed whether these correlates predict welfare better than range size per se, using data on captive juvenile mortality (from 13 518 individuals across 42 species) and stereotypic route-tracing (456 individuals, 27 species). Naturally itinerant lifestyles (quantified via ratios of daily to annual travel distances) were found to confer risk, predicting greater captive juvenile losses and stereotypic time-budgets. This finding advances our understanding of the evolutionary basis for welfare problems in captive Carnivora, helping explain why naturally sedentary species (e.g. American mink) may breed even in intensive farm conditions, while others (e.g. polar bears, giant pandas) can struggle even in modern zoos and conservation breeding centres. Naturally itinerant lifestyles involve decision-making, and strategic shifts between locations, suggesting that supplying more novelty, cognitive challenge and/or opportunities for control will be effective ways to meet these animals' welfare needs in captivity.

Polyploidy increases storage but decreases structural stability in Arabidopsis thaliana.

Whole-genome duplication, leading to polyploidy and endopolyploidy, is widespread throughout the tree of life.1-3 Both polyploidy and endopolyploidy can increase cell size via nucleotypic effects, but the phenotypic consequences of increased cell size at the tissue and whole-organism levels are less well understood.1-4 We quantified the consequences of autopolyploidy and endopolyploidy in nine diploid accessions of Arabidopsis thaliana, representing a gradient in endopolyploidy, to their corresponding experimentally synthesized neo-tetraploid and neo-octoploid cytotypes. The increase in cell size following genome duplication increased plant storage capacity, which increased tolerance of resource limitation, but also incurred biomechanical costs because of a reduction in the amount of cell wall per unit tissue volume. Our findings also show that the functional consequences of autopolyploidy can vary with accession identity, and the presence of this variation suggests that there is potential for adaptation following whole-genome duplication.

A meta-analysis of the effects of climate change on the mutualism between plants and arbuscular mycorrhizal fungi.

Climate change and other anthropogenic activities have the potential to alter the dynamics of resource exchange in the mutualistic symbiosis between plants and mycorrhizal fungi, potentially altering its stability. Arbuscular mycorrhizal (AM) fungi, which interact with most plant species, are less cold-tolerant than other groups of fungi; warming might therefore lead to increased fungal-mediated nutrient transfers to plants, which could strengthen the mutualism. By stimulating photosynthesis, rising CO2 could reduce the carbon cost of supporting AM fungi, which may also strengthen the mutualism. Furthermore, rising temperature and CO2 could have stronger effects on the mutualism in wild plants than in domesticated plants because the process of domestication can reduce the dependence of plants on mycorrhizal fungi. We conducted a multi-level random effects meta-analysis of experiments that quantified the strength of the mutualism as plant growth response to AM fungal inoculation (i.e., mycorrhizal growth response) under contrasting temperature and CO2 treatments that spanned the Last Glacial Maximum (LGM) to those expected with future climate change. We tested predictions using a three-level mixed effects meta-regression model with temperature or CO2, domestication status and their interaction as moderators. Increases from subambient to ambient temperature stimulated mycorrhizal growth response only for wild, but not for domesticated plant species. An increase from ambient to superambient temperature stimulated mycorrhizal growth response in both wild and domesticated plants, but the overall temperature effect was not statistically significant. By contrast, increased CO2 concentration, either from subambient to ambient or ambient to super ambient levels, did not affect mycorrhizal growth response in wild or domesticated plants. These results suggest the mutualism between wild plants and AM fungi was likely strengthened as temperature rose from the past to the present and that forecasted warming due to climate change may have modest positive effects on the mutualistic responses of plants to AM fungi. Mutualistic benefits obtained by plants from AM fungi may not have been altered by atmospheric CO2 increases from the past to the present, nor are they likely to be affected by a forecasted CO2 increase. This meta-analysis also identified gaps in the literature. In particular, (i) a large majority of studies that examined temperature effects on the mutualism focus on domesticated species (>80% of all trials) and (ii) very few studies examine how rising temperature and CO2, or other anthropogenic effects, interact to influence the mutualism. Therefore, to predict the stability of the mycorrhizal mutualism in the Anthropocene, future work should prioritize wild plant species as study subjects and focus on identifying how climate change factors and other human activities interact to affect plant responses to AM fungi.

Population-level variation in host plant response to multiple microbial mutualists.

PREMISE: Multipartite mutualisms are widespread in nature, but population-level variation in these interactions is rarely quantified. In the model multipartite mutualism between legumes, arbuscular mycorrhizal (AM) fungi and rhizobia bacteria, host responses to microbial partners are expected to be synergistic because the nutrients provided by each microbe colimit plant growth, but tests of this prediction have not been done in multiple host populations. METHODS: To test whether plant response to associations with AM fungi and rhizobia varies among host populations and whether synergistic responses to microbial mutualists are common, we grew 34 Medicago truncatula populations in a factorial experiment that manipulated the presence or absence of each mutualist. RESULTS: Plant growth increased in response to each mutualist, but there were no synergistic effects. Instead, plant response to inoculation with AM fungi was an order of magnitude higher than with rhizobia. Plant response to AM fungi varied among populations, whereas responses to rhizobia were relatively uniform. There was a positive correlation between plant host response to each mutualist but no correlation between AM fungal colonization and rhizobia nodulation of plant roots. CONCLUSIONS: The greater population divergence in host response to AM fungi relative to rhizobia, weak correlation in host response to each microbial mutualist, and the absence of a correlation between measures of AM fungal and rhizobia performance suggests that each plant-microbe mutualism evolved independently among M. truncatula populations.

Endopolyploidy is associated with leaf functional traits and climate variation in Arabidopsis thaliana.

PREMISE: Endopolyploidy is widespread throughout the tree of life and is especially prevalent in herbaceous angiosperms. Its prevalence in this clade suggests that endopolyploidy may be adaptive, but its functional roles are poorly understood. To address this gap in knowledge, we explored whether endopolyploidy was associated with climatic factors and correlated with phenotypic traits related to growth. METHODS: We sampled stem and leaf endopolyploidy in 56 geographically separated accessions of Arabidopsis thaliana grown in a common garden to explore species variation and to determine whether this variation was correlated with climatic variables and other plant traits. RESULTS: Stem endopolyploidy was not associated with climate or other traits. However, leaf endopolyploidy was significantly higher in accessions from drier and colder environments. Moreover, leaf endopolyploidy was positively correlated with apparent chlorophyll content and leaf dry mass. CONCLUSIONS: Endopolyploidy may have a functional role in the storage of chloroplasts and starch, and it may offer an adaptive avenue of tissue growth in cold and dry environments.

Independent evolutionary changes in fine-root traits among main clades during the diversification of seed plants.

Changes in fine-root morphology are typically associated with transitions from the ancestral arbuscular mycorrhizal (AM) to the alternative ectomycorrhizal (ECM) or nonmycorrhizal (NM) associations. However, the modifications in root morphology may also coincide with new modifications in leaf hydraulics and growth habit during angiosperm diversification. These hypotheses have not been evaluated concurrently, and this limits our understanding of the causes of fine-root evolution. To explore the evolution of fine-root systems, we assembled a 600+ species database to reconstruct historical changes in seed plants over time. We utilise ancestral reconstruction approaches together with phylogenetically informed comparative analyses to test whether changes in fine-root traits were most strongly associated with mycorrhizal affiliation, leaf hydraulics or growth form. Our findings showed significant shifts in root diameter, specific root length and root tissue density as angiosperms diversified, largely independent from leaf changes or mycorrhizal affiliation. Growth form was the only factor associated with fine-root traits in statistical models including mycorrhizal association and leaf venation, suggesting substantial modifications in fine-root morphology during transitions from woody to nonwoody habits. Divergences in fine-root systems were crucial in the evolution of seed plant lineages, with important implications for ecological processes in terrestrial ecosystems.

The influence of experimentally induced polyploidy on the relationships between endopolyploidy and plant function in Arabidopsis thaliana.

Whole genome duplication, leading to polyploidy and endopolyploidy, occurs in all domains and kingdoms and is especially prevalent in vascular plants. Both polyploidy and endopolyploidy increase cell size, but it is unclear whether both processes have similar effects on plant morphology and function, or whether polyploidy influences the magnitude of endopolyploidy. To address these gaps in knowledge, fifty-five geographically separated diploid accessions of Arabidopsis thaliana that span a gradient of endopolyploidy were experimentally manipulated to induce polyploidy. Both the diploids and artificially induced tetraploids were grown in a common greenhouse environment and evaluated with respect to nine reproductive and vegetative characteristics. Induced polyploidy decreased leaf endopolyploidy and stem endopolyploidy along with specific leaf area and stem height, but increased days to bolting, leaf size, leaf dry mass, and leaf water content. Phenotypic responses to induced polyploidy varied significantly among accessions but this did not affect the relationship between phenotypic traits and endopolyploidy. Our results provide experimental support for a trade-off between induced polyploidy and endopolyploidy, which caused induced polyploids to have lower endopolyploidy than diploids. Though polyploidy did not influence the relationship between endopolyploidy and plant traits, phenotypic responses to experimental genome duplication could not be easily predicted because of strong cytotype by accession interactions.

Variation in mycorrhizal growth response influences competitive interactions and mechanisms of plant species coexistence.

Plant species vary in their growth response to arbuscular mycorrhizal (AM) fungi, with responses ranging from negative to positive. Differences in response to AM fungi may affect competition between plant species, influencing their ability to coexist. We hypothesized that positively responding species, whose growth is stimulated by AM fungi, will experience stronger intraspecific competition and weaker interspecific competition in soil containing AM fungi, while neutrally or negatively responding species should experience weaker intraspecific and stronger interspecific competition. We grew Plantago lanceolata, which responds positively to AM fungi, and Bromus inermis, which responds negatively to AM fungi, in an additive response surface competition experiment that varied the total density and relative frequency of each species. Plants were grown in sterilized background soil that had been inoculated with whole soil biota, which includes AM fungi, or a microbial wash, that contained other soil microbes but no AM fungi, or in sterilized soil that contained no biota. The positively responding P. lanceolata was more strongly limited by intraspecific than interspecific competition when AM fungi were present. By contrast, the presence of AM fungi decreased the strength of intraspecific competition experienced by the negatively responding B. inermis. Because AM fungi are almost always present in soil, strong intraspecific competition in positively responding species would prevent them from outcompeting species that respond neutrally or negatively to AM fungi. The potential for increased intraspecific competition to offset growth benefits of AM fungi could, therefore, be a stabilizing mechanism that promotes coexistence among plant species.

Local adaptation to mycorrhizal fungi in geographically close Lobelia siphilitica populations.

Mutualism between plants and arbuscular mycorrhizal (AM) fungi is common, and plant populations are expected to have adapted to the AM fungal communities occupying their roots. Tests of this hypothesis have frequently been done with plant populations that are tens to hundreds of kilometers apart. However, because AM fungal community composition differs at scales < 1 km, local adaptation of plant populations to AM fungi may occur at small spatial scales, but this prediction has not been tested. Furthermore, prior experiments do not often experimentally identify whether adaptation is related to specific mycorrhizal functions. To test for plant adaptation to AM fungal communities at small spatial scales, and whether adaptation is associated with the nutritional benefits that AM fungi provide to plants, we grew Lobelia siphilitica plants from two geographically close populations (1.4 km apart) in a greenhouse reciprocal transplant experiment with soil biota that either included (whole soil) or excluded AM fungi (microbial wash) at both low and high soil phosphorus availability. Though both plant populations responded positively to the presence of AM fungi in the whole soil biota treatment relative to the microbial wash treatment, the average growth response of plant populations to mycorrhizal fungi was highest when local populations were grown with local AM fungi. In addition, local adaptation was only observed in the presence of AM fungi at low phosphorus levels. Thus, local adaptation of plant populations to AM fungi is present at spatial scales that are much smaller than previously demonstrated and occurred primarily to enhance phosphorus acquisition.

Vestured pits and scalariform perforation plate morphology modify the relationships between angiosperm vessel diameter, climate and maximum plant height.

Shared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because wood is complex, various traits may interact to influence vessel function. Specifically, pit vesturing (lignified cell wall protuberances associated with bordered pits) and perforation plate morphology could alter the relationships between vessel diameter, climate and plant height. Using phylogenetically informed analyses, we tested for associations between vessel diameter, climate and maximum plant height across angiosperm species with different pit vesturing (presence/absence) and perforation plate morphology (simple/scalariform and quantitative variation). We show significantly larger changes in vessel diameter and maximum plant height across climates for species with vestures and simple perforation plates, compared to nonvestured species and those with scalariform plates. We also found a significantly greater increase in height for a given increase in vessel diameter with lower percentage of scalariform plates. Our study provides novel insights into the evolution of angiosperm xylem by showing that vessel pit vesturing and perforation plate morphologies can modify relationships among xylem vessels, climate and height. Our findings highlight the complexity of xylem adaptations to climate, substantiating an integrative view of xylem function in the study of wood evolution.

Geographic range velocity and its association with phylogeny and life history traits in North American woody plants.

The geographic ranges of taxa change in response to environmental conditions. Yet whether rates of range movement (biotic velocities) are phylogenetically conserved is not well known. Phylogenetic conservatism of biotic velocities could reflect similarities among related lineages in climatic tolerances and dispersal-associated traits. We assess whether late Quaternary biotic velocities were phylogenetically conserved and whether they correlate with climatic tolerances and dispersal-associated traits. We used phylogenetic regression and nonparametric correlation to evaluate associations between biotic velocities, dispersal-associated traits, and climatic tolerances for 28 woody plant genera and subgenera in North America. The velocities with which woody plant taxa shifted their core geographic range limits were positively correlated from time step to time step between 16 and 7 ka. The strength of this correlation weakened after 7 ka as the pace of climate change slowed. Dispersal-associated traits and climatic tolerances were not associated with biotic velocities. Although the biotic velocities of some genera were consistently fast and others consistently slow, biotic velocities were not phylogenetically conserved. The rapid late Quaternary range shifts of plants lacking traits that facilitate frequent long-distance dispersal has long been noted (i.e., Reid's Paradox). Our results are consistent with this paradox and show that it remains robust when phylogenetic information is taken into account. The lack of association between biotic velocities, dispersal-associated traits, and climatic tolerances may reflect several, nonmutually exclusive processes, including rare long-distance dispersal, biotic interactions, and cryptic refugia. Because late Quaternary biotic velocities were decoupled from dispersal-associated traits, trait data for genera and subgenera cannot be used to predict longer-term (millennial-scale) floristic responses to climate change.

Does responsiveness to arbuscular mycorrhizal fungi depend on plant invasive status?

Differences in the direction and degree to which invasive alien and native plants are influenced by mycorrhizal associations could indicate a general mechanism of plant invasion, but whether or not such differences exist is unclear. Here, we tested whether mycorrhizal responsiveness varies by plant invasive status while controlling for phylogenetic relatedness among plants with two large grassland datasets. Mycorrhizal responsiveness was measured for 68 taxa from the Northern Plains, and data for 95 taxa from the Central Plains were included. Nineteen percent of taxa from the Northern Plains had greater total biomass with mycorrhizas while 61% of taxa from the Central Plains responded positively. For the Northern Plains taxa, measurable effects often depended on the response variable (i.e., total biomass, shoot biomass, and root mass ratio) suggesting varied resource allocation strategies when roots are colonized by arbuscular mycorrhizal fungi. In both datasets, invasive status was nonrandomly distributed on the phylogeny. Invasive taxa were mainly from two clades, that is, Poaceae and Asteraceae families. In contrast, mycorrhizal responsiveness was randomly distributed over the phylogeny for taxa from the Northern Plains, but nonrandomly distributed for taxa from the Central Plains. After controlling for phylogenetic similarity, we found no evidence that invasive taxa responded differently to mycorrhizas than other taxa. Although it is possible that mycorrhizal responsiveness contributes to invasiveness in particular species, we find no evidence that invasiveness in general is associated with the degree of mycorrhizal responsiveness. However, mycorrhizal responsiveness among species grown under common conditions was highly variable, and more work is needed to determine the causes of this variation.

Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth.

Although arbuscular mycorrhizal (AM) fungi are obligate symbionts that can influence plant growth, the magnitude and direction of these effects are highly variable within fungal genera and even among isolates within species, as well as among plant taxa. To determine whether variability in AM fungal morphology and growth is correlated with AM fungal effects on plant growth, we established a common garden experiment with 56 AM fungal isolates comprising 17 genera and six families growing with three plant host species. Arbuscular mycorrhizal fungal morphology and growth was highly conserved among isolates of the same species and among species within a family. By contrast, plant growth response to fungal inoculation was highly variable, with the majority of variation occurring among different isolates of the same AM fungal species. Our findings show that host performance cannot be predicted from AM fungal morphology and growth traits. Divergent effects on plant growth among isolates within an AM fungal species may be caused by coevolution between co-occurring fungal and plant populations.

Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics.

Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.

Arbuscular mycorrhizal fungi alter the competitive hierarchy among old-field plant species.

Inoculation with arbuscular mycorrhizal (AM) fungi is known to increase the species diversity of plant communities. One mechanism that can increase the likelihood of species co-existence, and thus species diversity, is a trade-off between competitive ability and the magnitude of plant growth response to AM fungal inoculation. By suppressing the growth of strong competitors while simultaneously enhancing the growth of weak competitors, this trade-off would cause the competitive hierarchy to be less pronounced in soil inoculated with AM fungi relative to non-inoculated conditions. To test whether such a trade-off exists, we quantified competitive abilities and mycorrhizal growth response (MGR) among 21 species that co-occur in old fields in southern Ontario. Competitive ability was determined by calculating competitive effect (CE), or the degree to which each species suppressed the biomass of a common phytometer species, Plantago lanceolata. Higher CE values represent stronger competitive ability. Old-field species varied in their ability to suppress the biomass of the phytometer and MGR was generally positive. There was a statistically significant negative correlation between CE in non-inoculated soil and MGR (r = -0.49, P = 0.02). In addition, variance in CE was 73% lower in soil inoculated with AM fungi compared to non-inoculated soil (P = 0.0023). These findings support the hypothesis that AM fungi weaken strong competitors while enhancing the performance of weak competitors. Because this trade-off compressed the competitive hierarchy among old-field species in soil inoculated with AM fungi, it may be a mechanism by which mycorrhizal fungi enhance species evenness and diversity.

Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis.

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.