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.

Microbial symbionts buffer hosts from the demographic costs of environmental stochasticity.

Species' persistence in increasingly variable climates will depend on resilience against the fitness costs of environmental stochasticity. Most organisms host microbiota that shield against stressors. Here, we test the hypothesis that, by limiting exposure to temporally variable stressors, microbial symbionts reduce hosts' demographic variance. We parameterized stochastic population models using data from a 14-year symbiont-removal experiment including seven grass species that host Epichloë fungal endophytes. Results provide novel evidence that symbiotic benefits arise not only through improved mean fitness, but also through dampened inter-annual variance. Hosts with "fast" life-history traits benefited most from symbiont-mediated demographic buffering. Under current climate conditions, contributions of demographic buffering were modest compared to benefits to mean fitness. However, simulations of increased stochasticity amplified benefits of demographic buffering and made it the more important pathway of host-symbiont mutualism. Microbial-mediated variance buffering is likely an important, yet cryptic, mechanism of resilience in an increasingly variable world.

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.

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.

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.

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.

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.

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.

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.

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.

Herbivore diet breadth mediates the cascading effects of carnivores in food webs.

Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex community of trees, caterpillars, and birds, we found a robust positive association between caterpillar diet breadth (phylodiversity of host plants used) and the strength of bird predation across 41 caterpillar and eight tree species. Dietary specialization was associated with increased enemy-free space for both camouflaged (n = 33) and warningly signaled (n = 8) caterpillar species. Furthermore, dietary specialization was associated with increased crypsis (camouflaged species only) and more stereotyped resting poses (camouflaged and warningly signaled species), but was unrelated to caterpillar body size. These dynamics in turn cascaded down to plants: a metaanalysis (n = 15 tree species) showed the beneficial effect of birds on trees (i.e., reduced leaf damage) decreased with the proportion of dietary specialist taxa composing a tree species' herbivore fauna. We conclude that herbivore diet breadth is a key functional trait underlying the trophic effects of carnivores on both herbivores and plants.

Quantitative trait locus mapping identifies candidate alleles involved in adaptive introgression and range expansion in a wild sunflower.

The wild North American sunflowers Helianthus annuus and H. debilis are participants in one of the earliest identified examples of adaptive trait introgression, and the exchange is hypothesized to have triggered a range expansion in H. annuus. However, the genetic basis of the adaptive exchange has not been examined. Here, we combine quantitative trait locus (QTL) mapping with field measurements of fitness to identify candidate H. debilis QTL alleles likely to have introgressed into H. annuus to form the natural hybrid lineage H. a. texanus. Two 500-individual BC1 mapping populations were grown in central Texas, genotyped for 384 single nucleotide polymorphism (SNP) markers and then phenotyped in the field for two fitness and 22 herbivore resistance, ecophysiological, phenological and architectural traits. We identified a total of 110 QTL, including at least one QTL for 22 of the 24 traits. Over 75% of traits exhibited at least one H. debilis QTL allele that would shift the trait in the direction of the wild hybrid H. a. texanus. We identified three chromosomal regions where H. debilis alleles increased both female and male components of fitness; these regions are expected to be strongly favoured in the wild. QTL for a number of other ecophysiological, phenological and architectural traits colocalized with these three regions and are candidates for the actual traits driving adaptive shifts. G × E interactions played a modest role, with 17% of the QTL showing potentially divergent phenotypic effects between the two field sites. The candidate adaptive chromosomal regions identified here serve as explicit hypotheses for how the genetic architecture of the hybrid lineage came into existence.

What we still don't know about invasion genetics.

Publication of The Genetics of Colonizing Species in 1965 launched the field of invasion genetics and highlighted the value of biological invasions as natural ecological and evolutionary experiments. Here, we review the past 50 years of invasion genetics to assess what we have learned and what we still don't know, focusing on the genetic changes associated with invasive lineages and the evolutionary processes driving these changes. We also suggest potential studies to address still-unanswered questions. We now know, for example, that rapid adaptation of invaders is common and generally not limited by genetic variation. On the other hand, and contrary to prevailing opinion 50 years ago, the balance of evidence indicates that population bottlenecks and genetic drift typically have negative effects on invasion success, despite their potential to increase additive genetic variation and the frequency of peak shifts. Numerous unknowns remain, such as the sources of genetic variation, the role of so-called expansion load and the relative importance of propagule pressure vs. genetic diversity for successful establishment. While many such unknowns can be resolved by genomic studies, other questions may require manipulative experiments in model organisms. Such studies complement classical reciprocal transplant and field-based selection experiments, which are needed to link trait variation with components of fitness and population growth rates. We conclude by discussing the potential for studies of invasion genetics to reveal the limits to evolution and to stimulate the development of practical strategies to either minimize or maximize evolutionary responses to environmental change.

Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis.

The hypothesis that interspecific hybridisation promotes invasiveness has received much recent attention, but tests of the hypothesis can suffer from important limitations. Here, we provide the first systematic review of studies experimentally testing the hybridisation-invasion (H-I) hypothesis in plants, animals and fungi. We identified 72 hybrid systems for which hybridisation has been putatively associated with invasiveness, weediness or range expansion. Within this group, 15 systems (comprising 34 studies) experimentally tested performance of hybrids vs. their parental species and met our other criteria. Both phylogenetic and non-phylogenetic meta-analyses demonstrated that wild hybrids were significantly more fecund and larger than their parental taxa, but did not differ in survival. Resynthesised hybrids (which typically represent earlier generations than do wild hybrids) did not consistently differ from parental species in fecundity, survival or size. Using meta-regression, we found that fecundity increased (but survival decreased) with generation in resynthesised hybrids, suggesting that natural selection can play an important role in shaping hybrid performance - and thus invasiveness - over time. We conclude that the available evidence supports the H-I hypothesis, with the caveat that our results are clearly driven by tests in plants, which are more numerous than tests in animals and fungi.

Responses of high-altitude graminoids and soil fungi to 20 years of experimental warming.

High-elevation ecosystems are expected to be particularly sensitive to climate warming because cold temperatures constrain biological processes. Deeper understanding of the consequences of climate change will come from studies that consider not only the direct effects of temperature on individual species, but also the indirect effects of altered species interactions. Here we show that 20 years of experimental warming has changed the species composition of graminoid (grass and sedge) assemblages in a subalpine meadow of the Rocky Mountains, USA, by increasing the frequency of sedges and reducing the frequency of grasses. Because sedges typically have weak interactions with mycorrhizal fungi relative to grasses, lowered abundances of arbuscular mycorrhizal (AM) fungi or other root-inhabiting fungi could underlie warming-induced shifts in plant species composition. However, warming increased root colonization by AM fungi for two grass species, possibly because AM fungi can enhance plant water uptake when soils are dried by experimental warming. Warming had no effect on AM fungal colonization of three other graminoids. Increased AM fungal colonization of the dominant shrub Artemisia tridentata provided further grounds for rejecting the hypothesis that reduced AM fungi caused the shift from grasses to sedges. Non-AM fungi (including dark septate endophytes) also showed general increases with warming. Our results demonstrate that lumping grasses and sedges when characterizing plant community responses can mask significant shifts in the responses of primary producers, and their symbiotic fungi, to climate change.

Sesquiterpene lactone stereochemistry influences herbivore resistance and plant fitness in the field.

BACKGROUND AND AIMS: Stereochemical variation is widely known to influence the bioactivity of compounds in the context of pharmacology and pesticide science, but our understanding of its importance in mediating plant-herbivore interactions is limited, particularly in field settings. Similarly, sesquiterpene lactones are a broadly distributed class of putative defensive compounds, but little is known about their activities in the field. METHODS: Natural variation in sesquiterpene lactones of the common cocklebur, Xanthium strumarium (Asteraceae), was used in conjunction with a series of common garden experiments to examine relationships between stereochemical variation, herbivore damage and plant fitness. KEY RESULTS: The stereochemistry of sesquiterpene lactone ring junctions helped to explain variation in plant herbivore resistance. Plants producing cis-fused sesquiterpene lactones experienced significantly higher damage than plants producing trans-fused sesquiterpene lactones. Experiments manipulating herbivore damage above and below ambient levels found that herbivore damage was negatively correlated with plant fitness. This pattern translated into significant fitness differences between chemotypes under ambient levels of herbivore attack, but not when attack was experimentally reduced via pesticide. CONCLUSIONS: To our knowledge, this work represents only the second study to examine sesquiterpene lactones as defensive compounds in the field, the first to document herbivore-mediated natural selection on sesquiterpene lactone variation and the first to investigate the ecological significance of the stereochemistry of the lactone ring junction. The results indicate that subtle differences in stereochemistry may be a major determinant of the protective role of secondary metabolites and thus of plant fitness. As stereochemical variation is widespread in many groups of secondary metabolites, these findings suggest the possibility of dynamic evolutionary histories within the Asteraceae and other plant families showing extensive stereochemical variation.

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.

Did genetic drift drive increases in genome complexity?

Mechanisms underlying the dramatic patterns of genome size variation across the tree of life remain mysterious. Effective population size (N(e)) has been proposed as a major driver of genome size: selection is expected to efficiently weed out deleterious mutations increasing genome size in lineages with large (but not small) N(e). Strong support for this model was claimed from a comparative analysis of N(e)u and genome size for ≈30 phylogenetically diverse species ranging from bacteria to vertebrates, but analyses at that scale have so far failed to account for phylogenetic nonindependence of species. In our reanalysis, accounting for phylogenetic history substantially altered the perceived strength of the relationship between N(e)u and genomic attributes: there were no statistically significant associations between N(e)u and gene number, intron size, intron number, the half-life of gene duplicates, transposon number, transposons as a fraction of the genome, or overall genome size. We conclude that current datasets do not support the hypothesis of a mechanistic connection between N(e) and these genomic attributes, and we suggest that further progress requires larger datasets, phylogenetic comparative methods, more robust estimators of genetic drift, and a multivariate approach that accounts for correlations between putative explanatory variables.