Plant-soil microbe feedbacks depend on distance and ploidy in a mixed cytotype population of Larrea tridentata.

PREMISE: Theory predicts that mixed ploidy populations should be short-lived due to strong fitness disadvantages for the rare ploidy. However, mixed ploidy populations are common, suggesting that the fitness costs for rare ploidies are counterbalanced by ecological benefits that emerge when rare. We investigated whether differences in ecological interactions with soil microbes help to maintain a tetraploid-hexaploid population of Larrea tridentata (creosote bush) in the Sonoran Desert, California, United States, where prior work documented ploidy-specific root-associated microbes. METHODS: We used a plant-soil feedback (PSF) experiment to test whether host-specific soil microbes can alter the outcomes of intraploidy vs. interploidy competition. Host-specific soil microbes can build up over time; thus, distance from a host plant can affect the fitness of nearby plants. RESULTS: Seedlings grown in soils from near plants of a different ploidy produced greater biomass relative to seedlings grown in soils from near plants of the same ploidy. Moreover, seedlings grown in soils from near plants of a different ploidy produced more biomass than those grown in soils that were farther from plants of a different ploidy. These results suggest that the ecological consequences of PSF may facilitate the persistence of mixed ploidy populations. CONCLUSIONS: This is the first evidence, to our knowledge, that is consistent with plant-soil microbe feedback as a viable mechanism to maintain the coexistence of multiple ploidy levels in a single population.

Heat and desiccation tolerances predict bee abundance under climate change.

Climate change could pose an urgent threat to pollinators, with critical ecological and economic consequences. However, for most insect pollinator species, we lack the long-term data and mechanistic evidence that are necessary to identify climate-driven declines and predict future trends. Here we document 16 years of abundance patterns for a hyper-diverse bee assemblage1 in a warming and drying region2, link bee declines with experimentally determined heat and desiccation tolerances, and use climate sensitivity models to project bee communities into the future. Aridity strongly predicted bee abundance for 71% of 665 bee populations (species × ecosystem combinations). Bee taxa that best tolerated heat and desiccation increased the most over time. Models forecasted declines for 46% of species and predicted more homogeneous communities dominated by drought-tolerant taxa, even while total bee abundance may remain unchanged. Such community reordering could reduce pollination services, because diverse bee assemblages typically maximize pollination for plant communities3. Larger-bodied bees also dominated under intermediate to high aridity, identifying body size as a valuable trait for understanding how climate-driven shifts in bee communities influence pollination4. We provide evidence that climate change directly threatens bee diversity, indicating that bee conservation efforts should account for the stress of aridity on bee physiology.

Why so many polyploids? Accounting for environmental stochasticity in unreduced gamete formation lowers the perceived barriers to polyploid establishment.

While polyploids are common in nature, existing models suggest that polyploid establishment should be difficult and rare. We explore this apparent paradox by focussing on the role of unreduced gametes, as their union is the main route for the formation of neopolyploids. Production of such gametes is affected by genetic and environmental factors, resulting in variation in the formation rate of unreduced gametes (u). Once formed, neopolyploids face minority cytotype exclusion (MCE) due to a lack of viable mating opportunities. More than a dozen theoretical models have explored factors that could permit neopolyploids to overcome MCE and become established. Until now, however, none have explored variability in u and its consequences for the rate of polyploid establishment. Here, we determine the distribution that best fits the available empirical data on u. We perform a global sensitivity analysis exploring the consequences of using empirical distributions of u to investigate effects on polyploid establishment. We determined that in many cases, u is best fit by a log-normal distribution. We found environmental stochasticity in u dramatically impacts model predictions when compared to a static u. Our results help reconcile previous modelling results suggesting high barriers to the polyploid establishment with the observation that polyploids are common in nature.

Grassland sensitivity to drought is related to functional composition across East Asia and North America.

Plant traits can be helpful for understanding grassland ecosystem responses to climate extremes, such as severe drought. However, intercontinental comparisons of how drought affects plant functional traits and ecosystem functioning are rare. The Extreme Drought in Grasslands experiment (EDGE) was established across the major grassland types in East Asia and North America (six sites on each continent) to measure variability in grassland ecosystem sensitivity to extreme, prolonged drought. At all sites, we quantified community-weighted mean functional composition and functional diversity of two leaf economic traits, specific leaf area and leaf nitrogen content, in response to drought. We found that experimental drought significantly increased community-weighted means of specific leaf area and leaf nitrogen content at all North American sites and at the wetter East Asian sites, but drought decreased community-weighted means of these traits at moderate to dry East Asian sites. Drought significantly decreased functional richness but increased functional evenness and dispersion at most East Asian and North American sites. Ecosystem drought sensitivity (percentage reduction in aboveground net primary productivity) positively correlated with community-weighted means of specific leaf area and leaf nitrogen content and negatively correlated with functional diversity (i.e., richness) on an intercontinental scale, but results differed within regions. These findings highlight both broad generalities but also unique responses to drought of community-weighted trait means as well as their functional diversity across grassland ecosystems.

Hybrid evolution repeats itself across environmental contexts in Texas sunflowers (Helianthus).

To what extent is evolution repeatable? Little is known about whether the evolution of hybrids is more (or less) repeatable than that of nonhybrids. We used field experimental evolution in annual sunflowers (Helianthus) in Texas to ask the extent to which hybrid evolution is repeatable across environments compared to nonhybrid controls. We created hybrids between Helianthus annuus (L.) and H. debilis (Nutt.) and grew plots of both hybrids and nonhybrid controls through eight generations at three sites in Texas. We collected seeds from each generation and grew each generation × treatment × home site combination at two final common gardens. We estimated the strength and direction of evolution in terms of fitness and 24 traits, tested for repeated versus nonrepeated evolution, and assessed overall phenotypic evolution across lineages and in relation to a locally adapted phenotype. Hybrids consistently evolved higher fitness over time, while controls did not, although trait evolution varied in strength across home sites. Repeated evolution was more evident in hybrids versus nonhybrid controls, and hybrid evolution was often in the direction of the locally adapted phenotype. Our findings have implications for both the nature of repeatability in evolution and the contribution of hybridization to evolution across environmental contexts.

Limited evidence for a positive relationship between hybridization and diversification across seed plant families.

Hybridization has experimental and observational ties to evolutionary processes and outcomes such as adaptation, speciation, and radiation. Although it has been hypothesized that hybridization and diversification are positively correlated, this idea remains largely untested empirically, and hybridization can also potentially reduce diversity. Here, we use a hybridization database on 170 seed plant families, life history information, and a time-calibrated phylogeny to test for phylogenetically-corrected associations between hybridization and diversification rates, while also taking into account life-history traits that may be correlated with both processes. We use three methods to estimate diversification rates and two metrics of hybridization. Although hybridization explains only a small amount of overall variation in diversification rates, we show that diversification and hybridization are sometimes positively correlated, although the effect sizes are very small. Moreover, the relationship remains detectable when incorporating the correlations between diversification and two other life history characteristics, perenniality and woodiness. We discuss potential mechanisms for this association under four different scenarios: hybridization may drive diversification, diversification may drive hybridization, both hybridization and diversification may jointly be driven by other factors, or, as an alternative, that there is in fact no relationship between the two. We suggest future studies to disentangle the causal structure.

Standing variation rather than recent adaptive introgression probably underlies differentiation of the texanus subspecies of Helianthus annuus.

The origins of geographic races in wide-ranging species are poorly understood. In Texas, the texanus subspecies of Helianthus annuus has long been thought to have acquired its defining phenotypic traits via introgression from a local congener, H. debilis, but previous tests of this hypothesis were inconclusive. Here, we explore the origins of H. a. texanus using whole genome sequencing data from across the entire range of H. annuus and possible donor species, as well as phenotypic data from a common garden study. We found that although it is morphologically convergent with H. debilis, H. a. texanus has conflicting signals of introgression. Genome wide tests (Patterson's D and TreeMix) only found evidence of introgression from H. argophyllus (sister species to H. annuus and also sympatric), but not H. debilis, with the exception of one individual of 109 analysed. We further scanned the genome for localized signals of introgression using PCAdmix and found minimal but nonzero introgression from H. debilis and significant introgression from H. argophyllus in some populations. Given the paucity of introgression from H. debilis, we argue that the morphological convergence observed in Texas is probably from standing genetic variation. We also found that genomic differentiation in H. a. texanus is mostly driven by large segregating inversions, several of which have signatures of natural selection based on haplotype frequencies.

Proximity to crop relatives determines some patterns of natural selection in a wild sunflower.

Abiotic and biotic heterogeneity result in divergent patterns of natural selection in nature, with important consequences for fundamental evolutionary processes including local adaptation, speciation, and diversification. However, increasing amounts of the global terrestrial surface are homogenized by agriculture (which covers nearly 50% of terrestrial vegetated land surface) and other anthropogenic activities. Agricultural intensification leads to highly simplified biotic communities for many taxa, which may alter natural selection through biotic selective agents. In particular, the presence of crops may alter selection on traits of closely related wild relatives via shared mutualists and antagonists such as pollinators and herbivores. We asked how the presence of crop sunflowers (Helianthus annuus) alters natural selection on reproductive traits of wild sunflowers (Helianthus annuus texanus). Across two years and multiple sites, we planted replicated paired populations of wild H. a. texanus bordering sunflower crop fields versus approximately 2.5 km away. We measured fitness, floral traits, and interactions of the plants with insect pollinators and seed predators. We found limited evidence that proximity to crop sunflowers altered selection on individual traits, as total or direct selection differed by proximity for only three of eleven traits: ray length (a marginally significant effect), Isophrictis (Gelechiidae, moth) attack, and Neolasioptera (Cecidomyiidae, midge) attack. Direct (but not total) selection was significantly more heterogenous far from crop sunflowers relative to near crop sunflowers. Both mutualist pollinators and antagonist seed predators mediated differences in selection in some population-pairs near versus far from crop sunflowers. Here, we demonstrate that agriculture can influence the evolution of wild species via altered selection arising from shared biotic interactions, complementing previously demonstrated evolutionary effects via hybridization.

Patterns, Predictors, and Consequences of Dominance in Hybrids.

AbstractCompared to those of their parents, are the traits of first-generation (F1) hybrids typically intermediate, biased toward one parent, or mismatched for alternative parental phenotypes? To address this empirical gap, we compiled data from 233 crosses in which traits were measured in a common environment for two parent taxa and their F1 hybrids. We find that individual traits in F1s are halfway between the parental midpoint and one parental value. Considering pairs of traits together, a hybrid's bivariate phenotype tends to resemble one parent (parent bias) about 50% more than the other, while also exhibiting a similar magnitude of mismatch due to different traits having dominance in conflicting directions. Using data from an experimental field planting of recombinant hybrid sunflowers, we illustrate that parent bias improves fitness, whereas mismatch reduces fitness. Our study has three major conclusions. First, hybrids are not phenotypically intermediate but rather exhibit substantial mismatch. Second, dominance is likely determined by the idiosyncratic evolutionary trajectories of individual traits and populations. Finally, selection against hybrids likely results from selection against both intermediate and mismatched phenotypes.

Birds Perceive More Intraspecific Color Variation in Bird-Pollinated Than Bee-Pollinated Flowers.

Pollinator-mediated selection is expected to constrain floral color variation within plant populations. Here, we test for patterns of constraint on floral color variation in 38 bee- and/or hummingbird-pollinated plant species from Colorado, United States. We collected reflectance spectra for at least 15 individuals in each of 1-3 populations of each species (total 78 populations) and modeled perceived color variation in both bee and bird visual spaces. We hypothesized that bees would perceive less intraspecific color variation in bee-pollinated species (vs. bird-pollinated species), and reciprocally, birds would perceive less color variation in bird-pollinated species (vs. bee-pollinated species). In keeping with the higher dimensionality of the bird visual system, birds typically perceived much more color variation than bees, regardless of plant pollination system. Contrary to our hypothesis, bees perceived equal color variation within plant species from the two pollination systems, and birds perceived more color variation in species that they pollinate than in bee-pollinated species. We propose hypotheses to account for the results, including reduced long-wavelength sensitivity in bees (vs. birds), and the ideas that potential categorical color vision in birds and larger cognitive capacities of birds (vs. bees) reduces their potential discrimination against floral color variants in species that they pollinate, resulting in less stabilizing selection on color within bird-pollinated vs. bee-pollinated species.

Predicting changes in bee assemblages following state transitions at North American dryland ecotones.

Drylands worldwide are experiencing ecosystem state transitions: the expansion of some ecosystem types at the expense of others. Bees in drylands are particularly abundant and diverse, with potential for large compositional differences and seasonal turnover across ecotones. To better understand how future ecosystem state transitions may influence bees, we compared bee assemblages and their seasonality among sites at the Sevilleta National Wildlife Refuge (NM, USA) that represent three dryland ecosystem types (and two ecotones) of the southwestern U.S. (Plains grassland, Chihuahuan Desert grassland, and Chihuahuan Desert shrubland). Using passive traps, we caught bees during two-week intervals from March-October, 2002-2014. The resulting dataset included 302 bee species and 56 genera. Bee abundance, composition, and diversity differed among ecosystems, indicating that future state transitions could alter bee assemblage composition in our system. We found strong seasonal bee species turnover, suggesting that bee phenological shifts may accompany state transitions. Common species drove the observed trends, and both specialist and generalist bee species were indicators of ecosystem types or months; these species could be sentinels of community-wide responses to future shifts. Our work suggests that predicting the consequences of global change for bee assemblages requires accounting for both within-year and among-ecosystem variation.

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community.

The enemy-free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple-predator types, raising the question of how so-called multiple-predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density- or frequency-dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life-history trade-offs associated with herbivore diet breadth.

Correlates of hybridization in plants.

Hybridization is a biological phenomenon increasingly recognized as an important evolutionary process in both plants and animals, as it is linked to speciation, radiation, extinction, range expansion and invasion, and allows for increased trait diversity in agricultural and horticultural systems. Estimates of hybridization frequency vary across taxonomic groups, but causes of this variation are unknown. Here, we ask on a global scale whether hybridization is linked to any of 11 traits related to plant life history, reproduction, genetic predisposition, and environment or opportunity. Given that hybridization is not evenly distributed across the plant tree of life, we use phylogenetic generalized least squares regression models and phylogenetic path analysis to detect statistical associations between hybridization and plant traits at both the family and genus levels. We find that perenniality and woodiness are each weakly associated with an increased frequency of hybridization in univariate analyses, but path analysis suggests that the direct linkage is between perenniality and increased hybridization (with woodiness having only an indirect relationship with hybridization via perenniality). Weak associations between higher rates of hybridization and higher outcrossing rates, abiotic pollination syndromes, vegetative reproductive modes, larger genomes, and less variable genome sizes are detectable in some cases but not others. We argue that correlational evidence at the global scale, such as that presented here, provides a robust framework for forming hypotheses to examine and test drivers of hybridization at a more mechanistic level.

No evidence that warmer temperatures are associated with selection for smaller body sizes.

Reductions in animal body size over recent decades are often interpreted as an adaptive evolutionary response to climate warming. However, for reductions in size to reflect adaptive evolution, directional selection on body size within populations must have become negative, or where already negative, to have become more so, as temperatures increased. To test this hypothesis, we performed traditional and phylogenetic meta-analyses of the association between annual estimates of directional selection on body size from wild populations and annual mean temperatures from 39 longitudinal studies. We found no evidence that warmer environments were associated with selection for smaller size. Instead, selection consistently favoured larger individuals, and was invariant to temperature. These patterns were similar in ectotherms and endotherms. An analysis using year rather than temperature revealed similar patterns, suggesting no evidence that selection has changed over time, and also indicating that the lack of association with annual temperature was not an artefact of choosing an erroneous time window for aggregating the temperature data. Although phenotypic trends in size will be driven by a combination of genetic and environmental factors, our results suggest little evidence for a necessary ingredient-negative directional selection-for declines in body size to be considered an adaptive evolutionary response to changing selection pressures.

Hybridization speeds adaptive evolution in an eight-year field experiment.

Hybridization is a common phenomenon, yet its evolutionary outcomes remain debated. Here, we ask whether hybridization can speed adaptive evolution using resynthesized hybrids between two species of Texas sunflowers (Helianthus annuus and H. debilis) that form a natural hybrid in the wild (H. annuus ssp. texanus). We established separate control and hybrid populations and allowed them to evolve naturally in a field evolutionary experiment. In a final common-garden, we measured fitness and a suite of key traits for these lineages. We show that hybrid fitness evolved in just seven generations, with fitness of the hybrid lines exceeding that of the controls by 14% and 51% by the end of the experiment, though only the latter represents a significant increase. More traits evolved significantly in hybrids relative to controls, and hybrid evolution was faster for most traits. Some traits in both hybrid and control lineages evolved in an adaptive manner consistent with the direction of phenotypic selection. These findings show a causal pathway from hybridization to rapid adaptation and suggest an explanation for the frequently noted association between hybridization and adaptive radiation, range expansion, and invasion.

Experimental drought reduces genetic diversity in the grassland foundation species Bouteloua eriopoda.

Understanding the resistance and resilience of foundation plant species to climate change is a critical issue because the loss of these species would fundamentally reshape communities and ecosystem processes. High levels of population genetic diversity may buffer foundation species against climate disruptions, but the strong selective pressures associated with climatic shifts may also rapidly reduce such diversity. We characterized genetic diversity and its responsiveness to experimental drought in the foundation plant, black grama grass (Bouteloua eriopoda), which dominates many western North American grasslands and shrublands. Previous studies suggested that in arid ecosystems, black grama reproduces largely asexually via stolons, and thus is likely to have low genetic variability, which might limit its potential to respond to climate disruptions. Using genotyping-by-sequencing, we demonstrated unexpectedly high genetic variability among black grama plants in a 1 ha site within the Sevilleta National Wildlife Refuge in central New Mexico, suggesting some level of sexual reproduction. Three years of experimental, growing season drought reduced black grama survival and biomass (the latter by 96%), with clear genetic differentiation (higher FST) between plants succumbing to drought and those remaining alive. Reduced genetic variability in the surviving plants in drought plots indicated that the experimental drought had forced black grama populations through selection bottlenecks. These results suggest that foundation grass species, such as black grama, may experience rapid evolutionary change if future climates include more severe droughts.

Phylogenetic trends and environmental correlates of nuclear genome size variation in Helianthus sunflowers.

Flowering plants serve as a powerful model for studying the evolution of nuclear genome size (GS) given the tremendous GS variation that exists both within and across angiosperm lineages. Helianthus sunflowers consist of c. 50 species native to North America that occupy diverse habitats and vary in ploidy level. In the current study, we generated a comprehensive GS database for 49 Helianthus species using flow cytometric approaches. We examined variability across the genus and present a comparative phylogenetic analysis of GS evolution in diploid Helianthus species. Results demonstrated that different clades of diploid Helianthus species showed evolutionary patterns of GS contraction, expansion and relative stasis, with annual diploid species evolving smaller GS with the highest rate of evolution. Phylogenetic comparative analyses of diploids revealed significant negative associations of GS with temperature seasonality and cell production rate, indicating that the evolution of larger GS in Helianthus diploids may be more permissible in habitats with longer growing seasons where selection for more rapid growth may be relaxed. The Helianthus GS database presented here and corresponding analyses of environmental and phenotypic correlates will facilitate ongoing and future research on the ultimate drivers of GS evolution in this well-studied North American plant genus.

A reassessment of the genome size-invasiveness relationship in reed canarygrass (Phalaris arundinacea).

Background and Aims: Genome size is hypothesized to affect invasiveness in plants. Key evidence comes from a previous study of invasive eastern North American populations of the grass Phalaris arundinacea: invasive genotypes with smaller genomes had higher growth rates, and genome sizes were smaller in the invasive vs. native range. This study aimed to re-investigate those patterns by examining a broader range of North American populations and by employing the modern best-practice protocol for plant genome size estimation in addition to the previously used protocol. Methods: Genome sizes were measured using both internal and pseudo-internal standardization protocols for 20 invasive and nine native range accessions of P. arundinacea. After a round of vegetative propagation to reduce maternal environmental effects, growth (stem elongation) rates of these accessions were measured in the greenhouse. Key Results: Using the best-practice protocol, there was no evidence of a correlation between genome size and growth rates (P = 0.704), and no evidence for differences in genome sizes of invasive and native range accessions (P > 0.353). However, using the older genome size estimation protocol, both relationships were significant (reproducing the results of the previous study). Conclusions: Genome size reduction has not driven increased invasiveness in a broad sample of North American P. arundinacea. Further, inappropriate genome size estimation techniques can create spurious correlations between genome size and plant traits such as growth rate. Valid estimation is vital to progress in understanding the potentially widespread effects of genome size on biological processes and patterns.

Vertically transmitted symbionts as mechanisms of transgenerational effects.

PREMISE OF THE STUDY: A transgenerational effect occurs when a biotic or abiotic environmental factor acts on a parental individual and thereby affects the phenotype of progeny. Due to the importance of transgenerational effects for understanding plant ecology and evolution, their underlying mechanisms are of general interest. Here, we introduce the concept that inherited symbiotic microorganisms could act as mechanisms of transgenerational effects in plants. METHODS: We define the criteria required to demonstrate that transgenerational effects are microbially mediated and review evidence from the well-studied, vertically transmitted plant-fungal symbiosis (grass-Epichloë spp.) in support of such effects. We also propose a basic experimental design to test for the presence of adaptive transgenerational effects mediated by plant symbionts. KEY RESULTS: An increasingly large body of literature shows that vertically transmitted microorganisms are common in plants, with potential to affect the phenotypes and fitness of progeny. Transgenerational effects could occur via parental modification of symbiont presence/absence, symbiont load, symbiont products, symbiont genotype or species composition, or symbiont priming. Several of these mechanisms appear likely in the grass-Epichloë endophytic symbiosis, as there is variation in the proportion of the progeny that carries the fungus, as well as variation in concentrations of mycelia and secondary compounds (alkaloids and osmolytes) in the seed. CONCLUSIONS: Symbiont-mediated transgenerational effects could be common in plants and could play large roles in plant adaptation to changing environments, but definitive tests are needed. We hope our contribution will spark new lines of research on the transgenerational effects of vertically transmitted symbionts in plants.