An evolutionary case for plant rarity: Eucalyptus as a model system.

Species rarity is a common phenomenon across global ecosystems that is becoming increasingly more common under climate change. Although species rarity is often considered to be a stochastic response to environmental and ecological constraints, we examined the hypothesis that plant rarity is a consequence of natural selection acting on performance traits that affect a species range size, habitat specificity, and population aggregation; three primary descriptors of rarity. Using a common garden of 25 species of Tasmanian Eucalyptus, we find that the rarest species have 70% lower biomass than common species. Although rare species demonstrate lower biomass, rare species allocated proportionally more biomass aboveground than common species. There is also a negative phylogenetic autocorrelation underlying the biomass of rare and common species, indicating that traits associated with rarity have diverged within subgenera as a result of environmental factors to reach different associated optima. In support of our hypothesis, we found significant positive relationships between species biomass, range size and habitat specificity, but not population aggregation. These results demonstrate repeated convergent evolution of the trait-based determinants of rarity across the phylogeny in Tasmanian eucalypts. Furthermore, the phylogenetically driven patterns in biomass and biomass allocation seen in rare species may be representative of a larger plant strategy, not yet considered, but offering a mechanism as to how rare species continue to persist despite inherent constraints of small, specialized ranges and populations. These results suggest that if rarity can evolve and is related to plant traits such as biomass, rather than a random outcome of environmental constraints, we may need to revise conservation efforts in these and other rare species to reconsider the abiotic and biotic factors that underlie the distributions of rare plant species.

Populations of western North American monkeyflowers accrue niche breadth primarily via genotypic divergence in environmental optima.

Niche breadth, the range of environments that individuals, populations, and species can tolerate, is a fundamental ecological and evolutionary property, yet few studies have examined how niche breadth is partitioned across biological scales. We use a published dataset of thermal performance for a single population from each of 10 closely related species of western North American monkeyflowers (genus Mimulus) to investigate whether populations achieve broad thermal niches through general purpose genotypes, specialized genotypes with divergent environmental optima, and/or variation among genotypes in the degree of generalization. We found the strongest relative support for the hypothesis that populations with greater genetic variation for thermal optimum had broader thermal niches, and for every unit increase in among-family variance in thermal optimum, population-level thermal breadth increased by 0.508°C. While the niche breadth of a single genotype represented up to 86% of population-level niche breadth, genotype-level niche breadth had a weaker positive effect on population-level breadth, with every 1°C increase in genotypic thermal breadth resulting in a 0.062°C increase in population breadth. Genetic variation for thermal breadth was not predictive of population-level thermal breadth. These findings suggest that populations of Mimulus species have achieved broad thermal niches primarily through genotypes with divergent thermal optima and to a lesser extent via general-purpose genotypes. Future work examining additional biological hierarchies would provide a more comprehensive understanding of how niche breadth partitioning impacts the vulnerabilities of individuals, populations, and species to environmental change.

Links Among Crop Diversification, Microbial Diversity, and Soil Organic Carbon: Mini Review and Case Studies.

Interactions between species above- and belowground are among the top factors that govern ecosystem functioning including soil organic carbon (SOC) storage. In agroecosystems, understanding how crop diversification affects soil biodiversity and SOC storage at the local scale remains a key challenge for addressing soil degradation and biodiversity loss that plague these systems. Yet, outcomes of crop diversification for soil microbial diversity and SOC storage, which are key indicators of soil health, are not always positive but rather they are highly idiosyncratic to agroecosystems. Using five case studies, we highlight the importance of selecting ideal crop functional types (as opposed to focusing on plant diversity) when considering diversification options for maximizing SOC accumulation. Some crop functional types and crop diversification approaches are better suited for enhancing SOC at particular sites, though SOC responses to crop diversification can vary annually and with duration of crop cover. We also highlight how SOC responses to crop diversification are more easily interpretable through changes in microbial community composition (as opposed to microbial diversity). We then develop suggestions for future crop diversification experiment standardization including (1) optimizing sampling effort and sequencing depth for soil microbial communities and (2) understanding the mechanisms guiding responses of SOC functional pools with varying stability to crop diversification. We expect that these suggestions will move knowledge forward about biodiversity and ecosystem functioning in agroecosystems, and ultimately be of use to producers for optimizing soil health in their croplands.

A viewpoint on ecological and evolutionary study of plant thermal performance curves in a warming world.

We can understand the ecology and evolution of plant thermal niches through thermal performance curves (TPCs), which are unimodal, continuous reaction norms of performance across a temperature gradient. Though there are numerous plant TPC studies, plants remain under-represented in syntheses of TPCs. Further, few studies quantify plant TPCs from fitness-based measurements (i.e. growth, survival and reproduction at the individual level and above), limiting our ability to draw conclusions from the existing literature about plant thermal adaptation. We describe recent plant studies that use a fitness-based TPC approach to test fundamental ecological and evolutionary hypotheses, some of which have uncovered key drivers of climate change responses. Then, we outline three conceptual questions in ecology and evolutionary biology for future plant TPC studies: (i) Do populations and species harbour genetic variation for TPCs? (ii) Do plant TPCs exhibit plastic responses to abiotic and biotic factors? (iii) Do fitness-based TPCs scale up to population-level thermal niches? Moving forward, plant ecologists and evolutionary biologists can capitalize on TPCs to understand how plasticity and adaptation will influence plant responses to climate change.

The evolution of thermal performance in native and invasive populations of Mimulus guttatus.

The rise of globalization has spread organisms beyond their natural range, allowing further opportunity for species to adapt to novel environments and potentially become invaders. Yet, the role of thermal niche evolution in promoting the success of invasive species remains poorly understood. Here, we use thermal performance curves (TPCs) to test hypotheses about thermal adaptation during the invasion process. First, we tested the hypothesis that if species largely conserve their thermal niche in the introduced range, invasive populations may not evolve distinct TPCs relative to native populations, against the alternative hypothesis that thermal niche and therefore TPC evolution has occurred in the invasive range. Second, we tested the hypothesis that clines of TPC parameters are shallower or absent in the invasive range, against the alternative hypothesis that with sufficient time, standing genetic variation, and temperature-mediated selection, invasive populations would re-establish clines found in the native range in response to temperature gradients. To test these hypotheses, we built TPCs for 18 native (United States) and 13 invasive (United Kingdom) populations of the yellow monkeyflower, Mimulus guttatus. We grew clones of multiple genotypes per population at six temperature regimes in growth chambers. We found that invasive populations have not evolved different thermal optima or performance breadths, providing evidence for evolutionary stasis of thermal performance between the native and invasive ranges after over 200 years post introduction. Thermal optimum increased with mean annual temperature in the native range, indicating some adaptive differentiation among native populations that was absent in the invasive range. Further, native and invasive populations did not exhibit adaptive clines in thermal performance breadth with latitude or temperature seasonality. These findings suggest that TPCs remained unaltered post invasion, and that invasion may proceed via broad thermal tolerance and establishment in already climatically suitable areas rather than rapid evolution upon introduction.

Spatial variation in high temperature-regulated gene expression predicts evolution of plasticity with climate change in the scarlet monkeyflower.

A major way that organisms can adapt to changing environmental conditions is by evolving increased or decreased phenotypic plasticity. In the face of current global warming, more attention is being paid to the role of plasticity in maintaining fitness as abiotic conditions change over time. However, given that temporal data can be challenging to acquire, a major question is whether evolution in plasticity across space can predict adaptive plasticity across time. In growth chambers simulating two thermal regimes, we generated transcriptome data for western North American scarlet monkeyflowers (Mimulus cardinalis) collected from different latitudes and years (2010 and 2017) to test hypotheses about how plasticity in gene expression is responding to increases in temperature, and if this pattern is consistent across time and space. Supporting the genetic compensation hypothesis, individuals whose progenitors were collected from the warmer-origin northern 2017 descendant cohort showed lower thermal plasticity in gene expression than their cooler-origin northern 2010 ancestors. This was largely due to a change in response at the warmer (40°C) rather than cooler (20°C) treatment. A similar pattern of reduced plasticity, largely due to a change in response at 40°C, was also found for the cooler-origin northern versus the warmer-origin southern population from 2017. Our results demonstrate that reduced phenotypic plasticity can evolve with warming and that spatial and temporal changes in plasticity predict one another.

A resurrection study reveals limited evolution of thermal performance in response to recent climate change across the geographic range of the scarlet monkeyflower.

Evolutionary rescue can prevent populations from declining under climate change, and should be more likely at high-latitude, "leading" edges of species' ranges due to greater temperature anomalies and gene flow from warm-adapted populations. Using a resurrection study with seeds collected before and after a 7-year period of record warming, we tested for thermal adaptation in the scarlet monkeyflower Mimulus cardinalis. We grew ancestors and descendants from northern-edge, central, and southern-edge populations across eight temperatures. Despite recent climate anomalies, populations showed limited evolution of thermal performance curves. However, one southern population evolved a narrower thermal performance breadth by 1.31°C, which matches the direction and magnitude of the average decrease in seasonality experienced. Consistent with the climate variability hypothesis, thermal performance breadth increased with temperature seasonality across the species' geographic range. Inconsistent with performance trade-offs between low and high temperatures across populations, we did not detect a positive relationship between thermal optimum and mean temperature. These findings fail to support the hypothesis that evolutionary response to climate change is greatest at the leading edge, and suggest that the evolution of thermal performance is unlikely to rescue most populations from the detrimental effects of rapidly changing climate.

Phylogeny is a powerful tool for predicting plant biomass responses to nitrogen enrichment.

Increasing rates of anthropogenic nitrogen (N) enrichment to soils often lead to the dominance of nitrophilic plant species and reduce plant diversity in natural ecosystems. Yet, we lack a framework to predict which species will be winners or losers in soil N enrichment scenarios, a framework that current literature suggests should integrate plant phylogeny, functional tradeoffs, and nutrient co-limitation. Using a controlled fertilization experiment, we quantified biomass responses to N enrichment for 23 forest tree species within the genus Eucalyptus that are native to Tasmania, Australia. Based on previous work with these species' responses to global change factors and theory on the evolution of plant resource-use strategies, we hypothesized that (1) growth responses to N enrichment are phylogenetically structured, (2) species with more resource-acquisitive functional traits have greater growth responses to N enrichment, and (3) phosphorus (P) limits growth responses to N enrichment differentially across species, wherein P enrichment increases growth responses to N enrichment more in some species than others. We built a hierarchical Bayesian model estimating effects of functional traits (specific leaf area, specific stem density, and specific root length) and P fertilization on species' biomass responses to N, which we then compared between lineages to determine whether phylogeny explains variation in responses to N. In concordance with literature on N limitation, a majority of species responded strongly and positively to N enrichment. Mean responses ranged three-fold, from 6.21 (E. pulchella) to 16.87 (E. delegatensis) percent increases in biomass per g N·m-2 ·yr-1 added. We identified a strong difference in responses to N between two phylogenetic lineages in the Eucalyptus subgenus Symphyomyrtus, suggesting that shared ancestry explains variation in N limitation. However, our model indicated that after controlling for phylogenetic non-independence, eucalypt responses to N were not associated with functional traits (although post-hoc analyses show a phylogenetic pattern in specific root length similar to that of responses to N), nor were responses differentially limited by P. Overall, our model results suggest that phylogeny is a powerful predictor of winners and losers in anthropogenic N enrichment scenarios in Tasmanian eucalypts, which may have implications for other species.

Phylogeny Explains Variation in The Root Chemistry of Eucalyptus Species.

Plants are dependent on their root systems for survival, and thus are defended from belowground enemies by a range of strategies, including plant secondary metabolites (PSMs). These compounds vary among species, and an understanding of this variation may provide generality in predicting the susceptibility of forest trees to belowground enemies and the quality of their organic matter input to soil. Here, we investigated phylogenetic patterns in the root chemistry of species within the genus Eucalyptus. Given the known diversity of PSMs in eucalypt foliage, we hypothesized that (i) the range and concentrations of PSMs and carbohydrates in roots vary among Eucalyptus species, and (ii) that phylogenetic relationships explain a significant component of this variation. To test for interspecific variation in root chemistry and the influence of tree phylogeny, we grew 24 Eucalyptus species representing two subgenera (Eucalyptus and Symphyomyrtus) in a common garden for two years. Fine root samples were collected from each species and analyzed for total phenolics, condensed tannins, carbohydrates, terpenes, and formylated phloroglucinol compounds. Compounds displaying significant interspecific variation were mapped onto a molecular phylogeny and tested for phylogenetic signal. Although all targeted groups of compounds were present, we found that phenolics dominated root defenses and that all phenolic traits displayed significant interspecific variation. Further, these compounds displayed a significant phylogenetic signal. Overall, our results suggest that within these representatives of genus Eucalyptus, more closely related species have more similar root chemistry, which may influence their susceptibility to belowground enemies and soil organic matter accrual.

Evolutionary history and novel biotic interactions determine plant responses to elevated CO2 and nitrogen fertilization.

A major frontier in global change research is predicting how multiple agents of global change will alter plant productivity, a critical component of the carbon cycle. Recent research has shown that plant responses to climate change are phylogenetically conserved such that species within some lineages are more productive than those within other lineages in changing environments. However, it remains unclear how phylogenetic patterns in plant responses to changing abiotic conditions may be altered by another agent of global change, the introduction of non-native species. Using a system of 28 native Tasmanian Eucalyptus species belonging to two subgenera, Symphyomyrtus and Eucalyptus, we hypothesized that productivity responses to abiotic agents of global change (elevated CO2 and increased soil N) are unique to lineages, but that novel interactions with a non-native species mediate these responses. We tested this hypothesis by examining productivity of 1) native species monocultures and 2) mixtures of native species with an introduced hardwood plantation species, Eucalyptus nitens, to experimentally manipulated soil N and atmospheric CO2. Consistent with past research, we found that N limits productivity overall, especially in elevated CO2 conditions. However, monocultures of species within the Symphyomyrtus subgenus showed the strongest response to N (gained 127% more total biomass) in elevated CO2 conditions, whereas those within the Eucalyptus subgenus did not respond to N. Root:shoot ratio (an indicator of resource use) was on average greater in species pairs containing Symphyomyrtus species, suggesting that functional traits important for resource uptake are phylogenetically conserved and explaining the phylogenetic pattern in plant response to changing environmental conditions. Yet, native species mixtures with E. nitens exhibited responses to CO2 and N that differed from those of monocultures, supporting our hypothesis and highlighting that both plant evolutionary history and introduced species will shape community productivity in a changing world.