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.

Microbial Inoculants: Silver Bullet or Microbial Jurassic Park?

The appeal of using microbial inoculants to mediate plant traits and productivity in managed ecosystems has increased over the past decade, because microbes represent an alternative to fertilizers, pesticides, and direct genetic modification of plants. Using microbes bypasses many societal and environmental concerns because microbial products are considered a more sustainable and benign technology. In our desire to harness the power of plant-microbial symbioses, are we ignoring the possibility of precipitating microbial invasions, potentially setting ourselves up for a microbial Jurassic Park? Here, we outline potential negative consequences of microbial invasions and describe a set of practices (Testing, Regulation, Engineering, and Eradication, TREE) based on the four stages of invasion to prevent microbial inoculants from becoming invasive. We aim to stimulate discussion about best practices to proactively prevent microbial invasions.

Microbe-mediated local adaptation to limestone barrens is context dependent.

Plant-root-associated microbes influence plant phenotype and tolerance to environmental stress, and thus have been hypothesized to play a role in plant local adaptation. Here, we test this hypothesis with factorial experiments addressing the role of microbes in local adaptation of Hypericum perforatum (St. John's wort) to stressful limestone barrens (alvars) compared to neighboring old-fields. Alvar plants benefited more from microbes in early life history stages, while at later growth stages, alvar and old-field plants benefited equally from microbes but only in the old-field habitat. Patterns of local adaptation were changed by the presence of microbes. Alvar plants grown in association with alvar microbes outperformed old-field plants in the alvar habitat, whereas old-field plants showed patterns of maladaptation when grown with microbes. In this demonstration of microbe-mediated adaptation, we show that rhizosphere microbes can be important for plant fitness and patterns of local adaptation but that those effects are dependent on life-history stage and habitat.

Gender Differences in Student Participation in an Active-Learning Classroom.

Overwhelming evidence demonstrating the benefits of active-learning pedagogy has led to a shift in teaching that requires students to interact more in the classroom. To date, few studies have assessed whether there are gender-specific differences in participation in active-learning science, technology, engineering, and mathematics (STEM) courses, and fewer have looked across different types of classroom participation. Over two semesters, we observed an introductory biology course at a large research-intensive university and categorized student participation into seven distinct categories to identify gender gaps in participation. Additionally, we collected student grades and administered a postcourse survey that gauged student scientific self-efficacy and salience of gender identity. We found that men participated more than expected based on the class composition in most participation categories. In particular, men were strongly overrepresented in voluntary responses after small-group discussions across both semesters. Women in the course reported lower scientific self-efficacy and greater salience of gender identity. Our results suggest that active learning in itself is not a panacea for STEM equity; rather, to maximize the benefits of active-learning pedagogy, instructors should make a concerted effort to use teaching strategies that are inclusive and encourage equitable participation by all students.

Herbivore removal reduces influence of arbuscular mycorrhizal fungi on plant growth and tolerance in an East African savanna.

The functional relationship between arbuscular mycorrhizal fungi (AMF) and their hosts is variable on small spatial scales. Here, we hypothesized that herbivore exclusion changes the AMF community and alters the ability of AMF to enhance plant tolerance to grazing. We grew the perennial bunchgrass, Themeda triandra Forssk in inoculum from soils collected in the Kenya Long-term Exclosure Experiment where treatments representing different levels of herbivory have been in place since 1995. We assessed AMF diversity in the field, using terminal restriction fragment length polymorphism and compared fungal diversity among treatments. We conducted clipping experiments in the greenhouse and field and assessed regrowth. Plants inoculated with AMF from areas accessed by wild herbivores and cattle had greater biomass than non-inoculated controls, while plants inoculated with AMF from where large herbivores were excluded did not benefit from AMF in terms of biomass production. However, only the inoculation with AMF from areas with wild herbivores and no cattle had a positive effect on regrowth, relative to clipped plants grown without AMF. Similarly, in the field, regrowth of plants after clipping in areas with only native herbivores was higher than other treatments. Functional differences in AMF were evident despite little difference in AMF species richness or community composition. Our findings suggest that differences in large herbivore communities over nearly two decades has resulted in localized, functional changes in AMF communities. Our results add to the accumulating evidence that mycorrhizae are locally adapted and that functional differences can evolve within small geographical areas.

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana.

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment-specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2-5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.

Effects of genetic perturbation on seasonal life history plasticity.

Like many species, the model plant Arabidopsis thaliana exhibits multiple different life histories in natural environments. We grew mutants impaired in different signaling pathways in field experiments across the species' native European range in order to dissect the mechanisms underlying this variation. Unexpectedly, mutational loss at loci implicated in the cold requirement for flowering had little effect on life history except in late-summer cohorts. A genetically informed photothermal model of progression toward flowering explained most of the observed variation and predicted an abrupt transition from autumn flowering to spring flowering in late-summer germinants. Environmental signals control the timing of this transition, creating a critical window of acute sensitivity to genetic and climatic change that may be common for seasonally regulated life history traits.