The evolutionary genomics of adaptation to stress in wild rhizobium bacteria.

Microbiota comprise the bulk of life's diversity, yet we know little about how populations of microbes accumulate adaptive diversity across natural landscapes. Adaptation to stressful soil conditions in plants provides seminal examples of adaptation in response to natural selection via allelic substitution. For microbes symbiotic with plants however, horizontal gene transfer allows for adaptation via gene gain and loss, which could generate fundamentally different evolutionary dynamics. We use comparative genomics and genetics to elucidate the evolutionary mechanisms of adaptation to physiologically stressful serpentine soils in rhizobial bacteria in western North American grasslands. In vitro experiments demonstrate that the presence of a locus of major effect, the nre operon, is necessary and sufficient to confer adaptation to nickel, a heavy metal enriched to toxic levels in serpentine soil, and a major axis of environmental soil chemistry variation. We find discordance between inferred evolutionary histories of the core genome and nreAXY genes, which often reside in putative genomic islands. This suggests that the evolutionary history of this adaptive variant is marked by frequent losses, and/or gains via horizontal acquisition across divergent rhizobium clades. However, different nre alleles confer distinct levels of nickel resistance, suggesting allelic substitution could also play a role in rhizobium adaptation to serpentine soil. These results illustrate that the interplay between evolution via gene gain and loss and evolution via allelic substitution may underlie adaptation in wild soil microbiota. Both processes are important to consider for understanding adaptive diversity in microbes and improving stress-adapted microbial inocula for human use.

Microbial mediation of salinity stress response varies by plant genotype and provenance over time.

Although it is becoming widely appreciated that microbes can enhance plant tolerance to environmental stress, the nature of microbial mediation of exposure responses is not well understood. We addressed this deficit by examining whether microbial mediation of plant responses to elevated salinity is contingent on the environment and factors intrinsic to the host. We evaluated the influence of contrasting environmental conditions relative to host genotype, provenance and evolution by conducting a common-garden experiment utilizing ancestral and descendant cohorts of Schoenoplectus americanus genotypes recovered from two 100+ year coastal marsh seed banks. We compared S. americanus productivity and trait variation as well as associated endophytic microbial communities according to plant genotype, provenance, and age cohort under high and low salinity stress with and without native soil inoculation. The magnitude and direction of microbial mediation of S. americanus responses to elevated salinity varied according to individual genotype, provenance, as well as temporal shifts in genotypic variation and G × E (gene by environment) interactions. Relationships differed between plant traits and the structure of endosphere communities. Our findings indicate that plant-microbe associations and microbial mediation of plant stress are not only context-dependent but also dynamic. Our results additionally suggest that evolution can shape the fate of marsh ecosystems by altering how microbes confer plant tolerance to pressures linked to global change.

The adaptive potential of plant populations in response to extreme climate events.

The frequency and magnitude of extreme climate events are increasing with global change, yet we lack predictions and empirical evidence for the ability of wild populations to persist and adapt in response to these events. Here, we used Fisher's Fundamental Theorem of Natural Selection to evaluate the adaptive potential of Lasthenia fremontii, a herbaceous winter annual that is endemic to seasonally flooded wetlands in California, to alternative flooding regimes that occur during El Niño Southern Oscillation (ENSO) events. The results indicate that populations may exhibit greater adaptive potential in response to dry years than wet years, and that the relative performance of populations will change across climate scenarios. More generally, our findings show that extreme climate events can substantially change the potential for populations to adapt to climate change by modulating the expression of standing genetic variation and mean fitness.

Grow Where You Thrive, or Where Only You Can Survive? An Analysis of Performance Curve Evolution in a Clade with Diverse Habitat Affinities.

Performance curves are valuable tools for quantifying the fundamental niches of organisms and testing hypotheses about evolution, life-history trade-offs, and the drivers of variation in species' distribution patterns. Here, we present a novel Bayesian method for characterizing performance curves that facilitates comparisons among species. We then use this model to quantify and compare the hydrological performance curves of 14 different taxa in the genus Lasthenia, an ecologically diverse clade of plants that collectively occupy a variety of habitats with unique hydrological features, including seasonally flooded wetlands called vernal pools. We conducted a growth chamber experiment to measure each taxon's fitness across five hydrological treatments that ranged from severe drought to extended flooding, and we identified differences in hydrological performance curves that explain their associations with vernal pool and terrestrial habitats. Our analysis revealed that the distribution of vernal pool taxa in the field does not reflect their optimal hydrological environments: all taxa, regardless of habitat affinity, have highest fitness under similar hydrological conditions of saturated soil without submergence. We also found that a taxon's relative position across flood gradients within vernal pools is best predicted by the height of its performance curve. These results demonstrate the utility of our approach for generating insights into when and how performance curves evolve among taxa as they diversify into distinct environments. To facilitate its use, the modeling framework has been developed into an R package.

Spatiotemporal heterogeneity in precipitation patterns explain population-level germination strategies in an edaphic specialist.

BACKGROUND AND AIMS: Many locally endemic species in biodiversity hotspots are restricted to edaphic conditions that are fixed in the landscape, limiting their potential to track climate change through dispersal. Instead, such species experience strong selection for germination strategies that can track suitable conditions through time. Germination strategies were compared among populations across the geographic range of a California vernal pool annual, Lasthenia fremontii Local germination strategies were tested to determine the associations with geographic variation in precipitation patterns. METHODS: This study evaluated patterns of seed germination, dormancy and mortality in response to simulated variation in the timing, amount and duration of the first autumn precipitation event using seeds from six populations that span a geographic gradient in precipitation. Next, it was tested whether the germination strategies of different populations can be predicted by historical precipitation patterns that characterize each site. KEY RESULTS: A significant positive relationship was observed between the historical variability in autumn precipitation and the extent of dormancy in a population. Marginal populations, with histories of the most extreme but constant autumn precipitation levels, expressed the lowest dormancy levels. Populations from sites with historically higher levels of autumn precipitation tended to germinate faster, but this tendency was not statistically significant. CONCLUSIONS: Germination in L. fremontii is cued by the onset of the first rains that characterize the beginning of winter in California's Great Central Valley. However, populations differ in how fast they germinate and the fraction of seeds that remain dormant when germination cues occur. The results suggest that seed dormancy may be a key trait for populations to track increasingly drier climates predicted by climate change models. However, the low dormancy and high mortality levels observed among seeds of the southernmost, driest populations make them most vulnerable to local extinction.

Competitive interference among rhizobia reduces benefits to hosts.

The capacity of beneficial microbes to compete for host infection-and the ability of hosts to discriminate among them-introduces evolutionary conflict that is predicted to destabilize mutualism. We investigated fitness outcomes in associations between legumes and their symbiotic rhizobia to characterize fitness impacts of microbial competition. Diverse Bradyrhizobium strains varying in their capacity to fix nitrogen symbiotically with a common host plant, Acmispon strigosus, were tested in full-factorial coinoculation experiments involving 28 pairwise strain combinations. We analyzed the effects of interstrain competition and host discrimination on symbiotic-interaction outcomes by relativizing fitness proxies to clonally infected and uninfected controls. More than one thousand root nodules of coinoculated plants were genotyped to quantify strain occupancy, and the Bradyrhizobium strain genome sequences were analyzed to uncover the genetic bases of interstrain competition outcomes. Strikingly, interstrain competition favored a fast-growing, minimally beneficial rhizobia strain. Host benefits were significantly diminished in coinoculation treatments relative to expectations from clonally inoculated controls, consistent with competitive interference among rhizobia that reduced both nodulation and plant growth. Competition traits appear polygenic, linked with inter-strain allelopathic interactions in the rhizosphere. This study confirms that competition among strains can destabilize mutualism by favoring microbes that are superior in colonizing host tissues but provide minimal benefits to host plants. Moreover, our findings help resolve the paradox that despite efficient host control post infection, legumes nonetheless encounter rhizobia that vary in their nitrogen fixation.

No disruption of rhizobial symbiosis during early stages of cowpea domestication.

Modern agriculture intensely selects aboveground plant structures, while often neglecting belowground features, and evolutionary tradeoffs between these traits are predicted to disrupt host control over microbiota. Moreover, drift, inbreeding, and relaxed selection for symbiosis in crops might degrade plant mechanisms that support beneficial microbes. We studied the impact of domestication on the nitrogen-fixing symbiosis between cowpea and root-nodulating Bradyrhizobium. We combined genome-wide analyses with a greenhouse inoculation study to investigate genomic diversity, heritability, and symbiosis trait variation among wild and early-domesticated cowpea genotypes. Cowpeas experienced modest decreases in genome-wide diversity during early domestication. Nonetheless, domesticated cowpeas responded efficiently to variation in symbiotic effectiveness, by forming more root nodules with nitrogen-fixing rhizobia and sanctioning nonfixing strains. Domesticated populations invested a larger proportion of host tissues into root nodules than wild cowpeas. Unlike soybean and wheat, cowpea showed no compelling evidence for degradation of symbiosis during domestication. Domesticated cowpeas experienced a less severe bottleneck than these crops and the low nutrient conditions in Africa where cowpea landraces were developed likely favored plant genotypes that gain substantial benefits from symbiosis. Breeders have largely neglected symbiosis traits, but artificial selection for improved plant responses to microbiota could increase plant performance and sustainability.

Evolution of specialization in a plant-microbial mutualism is explained by the oscillation theory of speciation.

Specialization in mutualisms is thought to be a major driver of diversification, but few studies have explored how novel specialization evolves, or its relation to the evolution of other niche axes. A fundamental question is whether generalist interactions evolve to become more specialized (i.e., oscillation hypothesis) or if partner switches evolve without any change in niche breadth (i.e., musical chairs hypothesis). We examined alternative models for the evolution of specialization by estimating the mutualistic, climatic, and edaphic niche breadths of sister plant species, combining phylogenetic, environmental, and experimental data on Acmispon strigosus and Acmispon wrangelianus genotypes across their overlapping ranges in California. We found that specialization along all three niche axes was asymmetric across species, such that the species with broader climatic and edaphic niches, Acmispon strigosus, was also able to gain benefit from and invest in associating with a broader set of microbial mutualists. Our data are consistent with the oscillation model of specialization, and a parallel narrowing of the edaphic, climatic, and mutualistic dimensions of the host species niche. Our findings provide novel evidence that the evolution of specialization in mutualism is accompanied by specialization in other niche dimensions.