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Macroclimate drives vegetation distributions, but fine-scale topographic variation can generate microclimate refugia for plant persistence in unsuitable areas. However, we lack quantitative descriptions of topography-driven microclimatic variation and how it shapes forest structure, diversity, and composition. We hypothesized that topographic variation and the presence of the forest overstory cause spatiotemporal microclimate variation affecting tree performance, causing forest structure, diversity, and composition to vary with topography and microclimate, and topography and the overstory to buffer microclimate. In a 20.2-ha inventory plot in the North American Great Plains, we censused woody stems ≥1 cm in diameter and collected detailed topographic and microclimatic data. Across 59-m of elevation, microclimate covaried with topography to create a sharp desiccation gradient, and topography and the overstory buffered understory microclimate. The magnitude of microclimatic variation mirrored that of regional-scale variation: with increasing elevation, there was a decrease in soil moisture corresponding to the difference across ~2.1° of longitude along the east-to-west aridity gradient and an increase in air temperature corresponding to the difference across ~2.7° of latitude along the north-to-south gradient. More complex forest structure and higher diversity occurred in moister, less-exposed habitats, and species occupied distinct topographic niches. Our study demonstrates how topographic and microclimatic gradients structure forests in putative climate-change refugia, by revealing ecological processes enabling populations to be maintained during periods of unfavorable macroclimate.
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Mycorrhizae, a form of plant-fungal symbioses, mediate vegetation impacts on ecosystem functioning. Climatic effects on decomposition and soil quality are suggested to drive mycorrhizal distributions, with arbuscular mycorrhizal plants prevailing in low-latitude/high-soil-quality areas and ectomycorrhizal (EcM) plants in high-latitude/low-soil-quality areas. However, these generalizations, based on coarse-resolution data, obscure finer-scale variations and result in high uncertainties in the predicted distributions of mycorrhizal types and their drivers. Using data from 31 lowland tropical forests, both at a coarse scale (mean-plot-level data) and fine scale (20 × 20 metres from a subset of 16 sites), we demonstrate that the distribution and abundance of EcM-associated trees are independent of soil quality. Resource exchange differences among mycorrhizal partners, stemming from diverse evolutionary origins of mycorrhizal fungi, may decouple soil fertility from the advantage provided by mycorrhizal associations. Additionally, distinct historical biogeographies and diversification patterns have led to differences in forest composition and nutrient-acquisition strategies across three major tropical regions. Notably, Africa and Asia's lowland tropical forests have abundant EcM trees, whereas they are relatively scarce in lowland neotropical forests. A greater understanding of the functional biology of mycorrhizal symbiosis is required, especially in the lowland tropics, to overcome biases from assuming similarity to temperate and boreal regions.
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Micorrizas , Árboles , Ecosistema , Suelo , NutrientesRESUMEN
Root hairs are considered important for rhizosphere formation, which affects root system functioning. Through interactions with soil microorganisms mediated by root exudation, root hairs may affect the phenotypes and growth of young plants. We tested this hypothesis by integrating results from two experiments: (1) a factorial greenhouse seedling experiment with Zea mays B73-wt and its root-hairless mutant, B73-rth3, grown in live and autoclaved soil, quantifying 15 phenotypic traits, seven growth rates, and soil microbiomes and (2) a semi-hydroponic system quantifying root exudation of maize genotypes. Possibly as compensation for lacking root hairs, B73-rth3 seedlings allocated more biomass to roots and grew slower than B73-wt seedlings in live soil, whereas B73-wt seedlings grew slowest in autoclaved soil, suggesting root hairs can be costly and their benefits were realized with more complete soil microbial assemblages. There were substantial differences in root exudation between genotypes and in rhizosphere versus non-rhizosphere microbiomes. The microbial taxa enriched in the presence of root hairs generally enhanced growth compared to taxa enriched in their absence. Our findings suggest the root hairs' adaptive value extends to plant-microbe interactions mediated by root exudates, affecting plant phenotypes, and ultimately, growth.
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Microbiota , Suelo , Plantones , Zea mays , Raíces de Plantas , Rizosfera , Microbiología del SueloRESUMEN
Plant genotype is recognized to contribute to variations in microbial community structure in the rhizosphere, soil adherent to roots. However, the extent to which the viral community varies has remained poorly understood and has the potential to contribute to variation in soil microbial communities. Here we cultivated replicates of two Zea mays genotypes, parviglumis and B73, in a greenhouse and harvested the rhizobiome (rhizoplane and rhizosphere) to identify the abundance of cells and viruses as well as rhizobiome microbial and viral community using 16S rRNA gene amplicon sequencing and genome resolved metagenomics. Our results demonstrated that viruses exceeded microbial abundance in the rhizobiome of parviglumis and B73 with a significant variation in both the microbial and viral community between the two genotypes. Of the viral contigs identified only 4.5% (n = 7) of total viral contigs were shared between the two genotypes, demonstrating that plants even at the level of genotype can significantly alter the surrounding soil viral community. An auxiliary metabolic gene associated with glycoside hydrolase (GH5) degradation was identified in one viral metagenome-assembled genome (vOTU) identified in the B73 rhizobiome infecting Propionibacteriaceae (Actinobacteriota) further demonstrating the viral contribution in metabolic potential for carbohydrate degradation and carbon cycling in the rhizosphere. This variation demonstrates the potential of plant genotype to contribute to microbial and viral heterogeneity in soil systems and harbors genes capable of contributing to carbon cycling in the rhizosphere.
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Plants influence the abiotic and biotic environment of the rhizosphere, affecting plant performance through plant-soil feedback (PSF). We compared the strength of nutrient and microbe-mediated PSF and its implications for plant performance in domesticated and wild grasses with a fully crossed greenhouse PSF experiment using four inbred maize genotypes (Zea mays ssp. mays b58, B73-wt, B73-rth3, and HP301), teosinte (Z. mays ssp. parviglumis), and two wild prairie grasses (Andropogon gerardii and Tripsacum dactyloides) to condition soils for three feedback species (maize B73-wt, teosinte, Andropogon gerardii). We found evidence of negative PSF based on growth, phenotypic traits, and foliar nutrient concentrations for maize B73-wt, which grew slower in maize-conditioned soil than prairie grass-conditioned soil. In contrast, teosinte and A. gerardii showed few consistent feedback responses. Both rhizobiome and nutrient-mediated mechanisms were implicated in PSF. Based on 16S rRNA gene amplicon sequencing, the rhizosphere bacterial community composition differed significantly after conditioning by prairie grass and maize plants, and the final soil nutrients were significantly influenced by conditioning, more so than by the feedback plants. These results suggest PSF-mediated soil domestication in agricultural settings can develop quickly and reduce crop productivity mediated by PSF involving changes to both the soil rhizobiomes and nutrient availability.
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Climate change is causing rapid shifts in the abiotic and biotic environmental conditions experienced by plant populations, but we lack generalizable frameworks for predicting the consequences for species. These changes may cause individuals to become poorly matched to their environments, potentially inducing shifts in the distributions of populations and altering species' habitat and geographic ranges. We present a trade-off-based framework for understanding and predicting whether plant species may undergo range shifts, based on ecological strategies defined by functional trait variation. We define a species' capacity for undergoing range shifts as the product of its colonization ability and the ability to express a phenotype well-suited to the environment across life stages (phenotype-environment matching), which are both strongly influenced by a species' ecological strategy and unavoidable trade-offs in function. While numerous strategies may be successful in an environment, severe phenotype-environment mismatches result in habitat filtering: propagules reach a site but cannot establish there. Operating within individuals and populations, these processes will affect species' habitat ranges at small scales, and aggregated across populations, will determine whether species track climatic changes and undergo geographic range shifts. This trade-off-based framework can provide a conceptual basis for species distribution models that are generalizable across plant species, aiding in the prediction of shifts in plant species' ranges in response to climate change.
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The Photochemical Reflectance Index (PRI) provides an optical indicator of photosynthetic light-use efficiency, photoprotection, and stress in plants. Although PRI can be applied in remote sensing, its interpretation depends on irradiance, which is hard to obtain from satellite or airborne imagery. To quantify forest photoprotective responses remotely, we developed a framework for modeling and interpreting PRI-light responses of individual trees and species using airborne imaging spectrometry coupled with georeferenced forest inventory data from a temperate broad-leaved forest. We derived an irradiance proxy, used hierarchical modeling to analyze PRI-light responses, and developed a framework of physiological interpretations of model parameters as facultative and constitutive components of photoprotection. Photochemical Reflectance Index declined with illumination, and PRI-light relationships varied with landscape position and among tree crowns and species. More sun-exposed foliage had lower intercepts and slopes of the relationship, indicating greater constitutive, but less facultative, photoprotection. We show that tree photoprotective strategies can be quantified at multiple scales using airborne hyperspectral data in structurally complex forests. Our findings and approach have important implications for the remote sensing of forest stress by offering a new way to assess functional diversity through dynamic differences in photoprotection and photosynthetic downregulation and providing previsual indicators of forest stress.
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Fotosíntesis , Árboles , Fotosíntesis/fisiología , Bosques , Plantas , Análisis Espectral , Hojas de la Planta/fisiologíaRESUMEN
[This corrects the article DOI: 10.1371/journal.pbio.3001674.].
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Climate change is having dramatic effects on the diversity and distribution of species. Many of these effects are mediated by how an organism's physiological patterns of resource allocation translate into fitness through effects on growth, survival and reproduction. Empirically, resource allocation is challenging to measure directly and so has often been approached using mathematical models, such as Dynamic Energy Budget (DEB) models. The fact that all plants require a very similar set of exogenous resources, namely light, water and nutrients, integrates well with the DEB framework in which a small number of variables and processes linked through pathways represent an organism's state as it changes through time. Most DEB theory has been developed in reference to animals and microorganisms. However, terrestrial vascular plants differ from these organisms in fundamental ways that make resource allocation, and the trade-offs and feedbacks arising from it, particularly fundamental to their life histories, but also challenging to represent using existing DEB theory. Here, we describe key features of the anatomy, morphology, physiology, biochemistry, and ecology of terrestrial vascular plants that should be considered in the development of a generic DEB model for plants. We then describe possible approaches to doing so using existing DEB theory and point out features that may require significant development for DEB theory to accommodate them. We end by presenting a generic DEB model for plants that accounts for many of these key features and describing gaps that would need to be addressed for DEB theory to predict the responses of plants to climate change. DEB models offer a powerful and generalizable framework for modelling resource allocation in terrestrial vascular plants, and our review contributes a framework for expansion and development of DEB theory to address how plants respond to anthropogenic change.
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Understanding tropical biology is important for solving complex problems such as climate change, biodiversity loss, and zoonotic pandemics, but biology curricula view research mostly via a temperate-zone lens. Integrating tropical research into biology education is urgently needed to tackle these issues.
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Biodiversidad , Cambio Climático , Biología , Clima TropicalRESUMEN
Seedling recruitment can be strongly affected by the composition of nearby plant species. At the neighborhood scale (on the order of tens of meters), adult conspecifics can modify soil chemistry and the presence of host microbes (pathogens and mutualists) across their combined canopy area or rooting zones. At local or small spatial scales (on the order of one to few meters), conspecific seed or seedling density can influence the strength of intraspecific light and resource competition and also modify the density-dependent spread of natural enemies such as pathogens or invertebrate predators. Intrinsic correlation between proximity to adult conspecifics (i.e., recruitment neighborhood) and local seedling density, arising from dispersal, makes it difficult to separate the independent and interactive factors that contribute to recruitment success. Here, we present a field experiment in which we manipulated both the recruitment neighborhood and seedling density to explore how they interact to influence the growth and survival of Dryobalanops aromatica, a dominant ectomycorrhizal tree species in a Bornean tropical rainforest. First, we found that both local seedling density and recruitment neighborhood had effects on performance of D. aromatica seedlings, though the nature of these impacts varied between growth and survival. Second, we did not find strong evidence that the effect of density on seedling survival is dependent on the presence of conspecific adult trees. However, accumulation of mutualistic fungi beneath conspecifics adults does facilitate establishment of D. aromatica seedlings. In total, our results suggest that recruitment near adult conspecifics was not associated with a performance cost and may have weakly benefitted recruiting seedlings. Positive effects of conspecifics may be a factor facilitating the regional hyperabundance of this species. Synthesis: Our results provide support for the idea that dominant species in diverse forests may escape the localized recruitment suppression that limits abundance in rarer species.
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Tree rings provide an invaluable long-term record for understanding how climate and other drivers shape tree growth and forest productivity. However, conventional tree-ring analysis methods were not designed to simultaneously test effects of climate, tree size, and other drivers on individual growth. This has limited the potential to test ecologically relevant hypotheses on tree growth sensitivity to environmental drivers and their interactions with tree size. Here, we develop and apply a new method to simultaneously model nonlinear effects of primary climate drivers, reconstructed tree diameter at breast height (DBH), and calendar year in generalized least squares models that account for the temporal autocorrelation inherent to each individual tree's growth. We analyze data from 3811 trees representing 40 species at 10 globally distributed sites, showing that precipitation, temperature, DBH, and calendar year have additively, and often interactively, influenced annual growth over the past 120 years. Growth responses were predominantly positive to precipitation (usually over ≥3-month seasonal windows) and negative to temperature (usually maximum temperature, over ≤3-month seasonal windows), with concave-down responses in 63% of relationships. Climate sensitivity commonly varied with DBH (45% of cases tested), with larger trees usually more sensitive. Trends in ring width at small DBH were linked to the light environment under which trees established, but basal area or biomass increments consistently reached maxima at intermediate DBH. Accounting for climate and DBH, growth rate declined over time for 92% of species in secondary or disturbed stands, whereas growth trends were mixed in older forests. These trends were largely attributable to stand dynamics as cohorts and stands age, which remain challenging to disentangle from global change drivers. By providing a parsimonious approach for characterizing multiple interacting drivers of tree growth, our method reveals a more complete picture of the factors influencing growth than has previously been possible.
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Cambio Climático , Bosques , Biomasa , Clima , TemperaturaRESUMEN
Tropical forest regeneration after abandonment of former agricultural land depends critically on the input of tree seeds, yet seed dispersal is increasingly disrupted in contemporary human-modified landscapes. Here, we introduce the concept of seed-rain-successional feedbacks as a deterministic process in which seed rain is shaped by successional dynamics internal to a forest site and that acts to reinforce priority effects. We used a combination of time series and chronosequence approaches to investigate how the quantity and taxonomic and functional composition of seed rain change during succession and to evaluate the strength of seed-rain-successional feedbacks, relative to other deterministic and stochastic mechanisms, in secondary wet forests of Costa Rica. We found that both successional niches and seed-rain-successional feedbacks shaped successional trajectories in the seed rain. Determinism due to successional niche assembly was supported by the increasing convergence of community structure to that of a mature forest, in terms of both functional and taxonomic composition. With successional age, the proportions of large-seeded, shade-tolerant species in the seed rain increased, whereas the proportion of animal-dispersed species did not change significantly. Seed-rain-successional feedbacks increased in strength with successional age, as the proportion of immigrant seeds (species not locally represented in the site) decreased with successional age, and the composition of the seed rain became more similar to that of the adult trees at the forest site. The deterministic assembly generated by seed-rain-successional feedback likely contributed to the increasing divergence of secondary forest sites from each other during succession. To the extent that human modification of tropical forest landscapes reduces connectivity via factors such as forest cover loss, our results suggest that seed-rain-successional feedbacks are likely to increasingly shape regeneration trajectories in and amplify floristic heterogeneity among tropical secondary forests.
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Bosques , Clima Tropical , Animales , Costa Rica , Retroalimentación , Humanos , Semillas , ÁrbolesRESUMEN
Resource allocation within trees is a zero-sum game. Unavoidable trade-offs dictate that allocation to growth-promoting functions curtails other functions, generating a gradient of investment in growth versus survival along which tree species align, known as the interspecific growth-mortality trade-off. This paradigm is widely accepted but not well established. Using demographic data for 1,111 tree species across ten tropical forests, we tested the generality of the growth-mortality trade-off and evaluated its underlying drivers using two species-specific parameters describing resource allocation strategies: tolerance of resource limitation and responsiveness of allocation to resource access. Globally, a canonical growth-mortality trade-off emerged, but the trade-off was strongly observed only in less disturbance-prone forests, which contained diverse resource allocation strategies. Only half of disturbance-prone forests, which lacked tolerant species, exhibited the trade-off. Supported by a theoretical model, our findings raise questions about whether the growth-mortality trade-off is a universally applicable organizing framework for understanding tropical forest community structure.
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Bosques , Clima Tropical , Especificidad de la Especie , ÁrbolesRESUMEN
Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant-soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF-hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF-hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF-hosting species had slower leaf economics than AMF-hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale-dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.
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Micorrizas , Bosques , Raíces de Plantas , Bosque Lluvioso , Suelo , Microbiología del Suelo , ÁrbolesRESUMEN
While work in temperate forests suggests that there are consistent differences in plant-soil feedback (PSF) between plants with arbuscular and ectomycorrhizal associations, it is unclear whether these differences exist in tropical rainforests. We tested the effects of mycorrhizal type, phylogenetic relationships to overstory species, and soil fertility on the growth of tree seedlings in a tropical Bornean rainforest with a high diversity of both ectomycorrhizal and arbuscular mycorrhizal trees. We found that ectomycorrhizal tree seedlings had higher growth in soils conditioned by close relatives and that this was associated with higher mycorrhizal colonization. By contrast, arbuscular mycorrhizal tree seedlings generally grew more poorly in soils conditioned by close relatives. For ectomycorrhizal species, the phylogenetic trend was insensitive to soil fertility. For arbuscular mycorrhizal seedlings, however, the effect of growing in soils conditioned by close relatives became increasingly negative as soil fertility increased. Our results demonstrate consistent effects of mycorrhizal type on plant-soil feedbacks across forest biomes. The positive effects of ectomycorrhizal symbiosis may help explain biogeographic variation across tropical forests, such as familial dominance of the Dipterocarpaceae in southeast Asia. However, positive feedbacks also raise questions about the role of PSFs in maintaining tropical diversity.
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Micorrizas , Retroalimentación , Bosques , Hongos , Micorrizas/genética , Filogenia , Suelo , Microbiología del SueloRESUMEN
The competition-colonization trade-off, by which species can partition spatial niches, is a potentially important mechanism allowing the maintenance of species diversity in plant communities. We examined whether there was evidence for this trade-off among tree species in a subtropical forest and how it correlated with eight functional traits. We developed and estimated a metric for colonization ability that incorporates both fecundity and seed dispersal based on seed trap data and the sizes and distributions of adult trees. Competitive ability was estimated as survival probability under high crowding conditions based on neighborhood models. Although we found no significant relationship between colonization and competitive abilities, there was a significant negative correlation between long distance dispersal ability and competitive ability at the 5 cm size class. Colonizers had traits associated with faster growth, such as large leaves and low leaf lamina density, whereas competitors had traits associated with higher survival, such as dense wood. Our results imply that any trade-off between competition and colonization may be more determined by dispersal ability than by fecundity, suggesting that seed dispersal is an important contributor to diversity maintenance. Future work should test how competitive ability covaries with the components of colonization ability, as we did here.
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Fagaceae/fisiología , Variación Genética , Juglandaceae/fisiología , Lauraceae/fisiología , Theaceae/fisiología , Árboles/fisiología , Bosques , Modelos Estadísticos , Fenotipo , Hojas de la Planta , Probabilidad , Dispersión de Semillas , Semillas , Especificidad de la Especie , MaderaRESUMEN
Stress memory refers to the observation that an initial, sub-lethal stress alters plants' responses to subsequent stresses. Previous transcriptome analyses of maize seedlings exposed to a repeated dehydration stress has revealed the existence of transcriptional stress memory in Zea mays. Whether drought-related physiological responses also display memory and how transcriptional memory translates into physiological memory are fundamental questions that are still unanswered. Using a systems-biology approach we investigate whether/how transcription memory responses established in the genome-wide analysis of Z. mays correlate with 14 physiological parameters measured during a repeated exposure of maize seedlings to dehydration stress. Co-expression network analysis revealed ten gene modules correlating strongly with particular physiological processes, and one module displaying strong, yet divergent, correlations with several processes suggesting involvement of these genes in coordinated responses across networks. Two processes key to the drought response, stomatal conductance and non-photochemical quenching, displayed contrasting memory patterns that may reflect trade-offs related to metabolic costs versus benefits of cellular protection. The main contribution of this study is the demonstration of coordinated changes in transcription memory responses at the genome level and integrated physiological responses at the cellular level upon repetitive stress exposures. The results obtained by the network-based systems analysis challenge the commonly held view that short-term physiological responses to stress are primarily mediated biochemically.
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Trees grow by vertically extending their stems, so accurate stem hydraulic models are fundamental to understanding the hydraulic challenges faced by tall trees. Using a literature survey, we showed that many tree species exhibit continuous vertical variation in hydraulic traits. To examine the effects of this variation on hydraulic function, we developed a spatially explicit, analytical water transport model for stems. Our model allows Huber ratio, stem-saturated conductivity, pressure at 50% loss of conductivity, leaf area, and transpiration rate to vary continuously along the hydraulic path. Predictions from our model differ from a matric flux potential model parameterized with uniform traits. Analyses show that cavitation is a whole-stem emergent property resulting from non-linear pressure-conductivity feedbacks that, with gravity, cause impaired water transport to accumulate along the path. Because of the compounding effects of vertical trait variation on hydraulic function, growing proportionally more sapwood and building tapered xylem with height, as well as reducing xylem vulnerability only at branch tips while maintaining transport capacity at the stem base, can compensate for these effects. We therefore conclude that the adaptive significance of vertical variation in stem hydraulic traits is to allow trees to grow tall and tolerate operating near their hydraulic limits.
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Tallos de la Planta/metabolismo , Trisacáridos/metabolismo , Agua/metabolismo , Xilema/metabolismo , Modelos BiológicosRESUMEN
Convergence occurs in both species traits and community structure, but how convergence at the two scales influences each other remains unclear. To address this question, we focus on tropical forest monodominance, in which a single, often ectomycorrhizal (EM) tree species occasionally dominates forest stands within a landscape otherwise characterized by diverse communities of arbuscular mycorrhizal (AM) trees. Such monodominance is a striking potential example of community divergence resulting in alternative stable states. However, it is observed only in some tropical regions. A diverse suite of AM and EM trees locally codominate forest stands elsewhere. We develop a hypothesis to explain this geographical difference using a simulation model of plant community assembly. Simulation results suggest that in a region with a few EM species (e.g., South America), EM trees experience strong selection for convergent traits that match the abiotic conditions of the environment. Consequently, EM species successfully compete against other species to form monodominant stands via positive plant-soil feedbacks. By contrast, in a region with many EM species (e.g., Southeast Asia), species maintain divergent traits because of complex plant-soil feedbacks, with no species having traits that enable monodominance. An analysis of plant trait data from Borneo and Peruvian Amazon was inconclusive. Overall, this work highlights the utility of geographical comparison in understanding the relationship between trait convergence and community convergence.