Increased hydraulic risk in assemblages of woody plant species predicts spatial patterns of drought-induced mortality.

Predicting drought-induced mortality (DIM) of woody plants remains a key research challenge under climate change. Here, we integrate information on the edaphoclimatic niches, phylogeny and hydraulic traits of species to model the hydraulic risk of woody plants globally. We combine these models with species distribution records to estimate the hydraulic risk faced by local woody plant species assemblages. Thus, we produce global maps of hydraulic risk and test for its relationship with observed DIM. Our results show that local assemblages modelled as having higher hydraulic risk present a higher probability of DIM. Metrics characterizing this hydraulic risk improve DIM predictions globally, relative to models accounting only for edaphoclimatic predictors or broad functional groupings. The methodology we present here allows mapping of functional trait distributions and elucidation of global macro-evolutionary and biogeographical patterns, improving our ability to predict potential global change impacts on vegetation.

Range restricted old and young lineages show the southern Western Ghats to be both a museum and a cradle of diversity for woody plants.

The Western Ghats (WG) mountain chain is a global biodiversity hotspot with high diversity and endemicity of woody plants. The latitudinal breadth of the WG offers an opportunity to determine the evolutionary drivers of latitudinal diversity patterns. We examined the spatial patterns of evolutionary diversity using complementary phylogenetic diversity and endemism measures. To examine if different regions of the WG serve as a museum or cradle of evolutionary diversity, we examined the distribution of 470 species based on distribution modelling and occurrence locations across the entire region. In accordance with the expectation, we found that the southern WG is both a museum and cradle of woody plant evolutionary diversity, as a higher proportion of both old and young evolutionary lineages are restricted to the southern WG. The diversity gradient is likely driven by high geo-climatic stability in the south and phylogenetic niche conservatism for moist and aseasonal sites. This is corroborated by persistent lineage nestedness at almost all evolutionary depths (10-135 million years), and a strong correlation of evolutionary diversity with drought seasonality, precipitation and topographic heterogeneity. Our results highlight the global value of the WG, demonstrating, in particular, the importance of protecting the southern WG-an engine of plant diversification and persistence.

Precipitation is the main axis of tropical plant phylogenetic turnover across space and time.

Early natural historians-Comte de Buffon, von Humboldt, and De Candolle-established environment and geography as two principal axes determining the distribution of groups of organisms, laying the foundations for biogeography over the subsequent 200 years, yet the relative importance of these two axes remains unresolved. Leveraging phylogenomic and global species distribution data for Mimosoid legumes, a pantropical plant clade of c. 3500 species, we show that the water availability gradient from deserts to rain forests dictates turnover of lineages within continents across the tropics. We demonstrate that 95% of speciation occurs within a precipitation niche, showing profound phylogenetic niche conservatism, and that lineage turnover boundaries coincide with isohyets of precipitation. We reveal similar patterns on different continents, implying that evolution and dispersal follow universal processes.

Diversity and divergence: evolution of secondary metabolism in the tropical tree genus Inga.

Plants are widely recognized as chemical factories, with each species producing dozens to hundreds of unique secondary metabolites. These compounds shape the interactions between plants and their natural enemies. We explore the evolutionary patterns and processes by which plants generate chemical diversity, from evolving novel compounds to unique chemical profiles. We characterized the chemical profile of one-third of the species of tropical rainforest trees in the genus Inga (c. 100, Fabaceae) using ultraperformance liquid chromatography-mass spectrometry-based metabolomics and applied phylogenetic comparative methods to understand the mode of chemical evolution. We show: each Inga species contain structurally unrelated compounds and high levels of phytochemical diversity; closely related species have divergent chemical profiles, with individual compounds, compound classes, and chemical profiles showing little-to-no phylogenetic signal; at the evolutionary time scale, a species' chemical profile shows a signature of divergent adaptation. At the ecological time scale, sympatric species were the most divergent, implying it is also advantageous to maintain a unique chemical profile from community members; finally, we integrate these patterns with a model for how chemical diversity evolves. Taken together, these results show that phytochemical diversity and divergence are fundamental to the ecology and evolution of plants.

Dissecting the difference in tree species richness between Africa and South America.

SignificanceOur full-scale comparison of Africa and South America's lowland tropical tree floras shows that both Africa and South America's moist and dry tree floras are organized similarly: plant families that are rich in tree species on one continent are also rich in tree species on the other continent, and these patterns hold across moist and dry environments. Moreover, we confirm that there is an important difference in tree species richness between the two continents, which is linked to a few families that are exceptionally diverse in South American moist forests, although dry formations also contribute to this difference. Plant families only present on one of the two continents do not contribute substantially to differences in tree species richness.

Climatic niche lability but growth form conservatism in the African woody flora.

Climatic niche evolution during the diversification of tropical plants has received little attention in Africa. To address this, we characterised the climatic niche of >4000 tropical African woody species, distinguishing two broad bioclimatic groups (forest vs. savanna) and six subgroups. We quantified niche conservatism versus lability at the genus level and for higher clades, using a molecular phylogeny of >800 genera. Although niche stasis at speciation is prevalent, numerous clades individually cover vast climatic spaces suggesting a general ease in transcending ecological limits, especially across bioclimatic subgroups. The forest biome was the main source of diversity, providing many lineages to savanna, but reverse shifts also occurred. We identified clades that diversified in savanna after shifts from forest. The forest-savanna transition was not consistently associated with a growth form change, though we found evolutionarily labile clades whose presence in forest or savanna is associated respectively with climbing or shrubby species diversification.

Structural diversity and tree density drives variation in the biodiversity-ecosystem function relationship of woodlands and savannas.

Positive biodiversity-ecosystem function relationships (BEFRs) have been widely documented, but it is unclear if BEFRs should be expected in disturbance-driven systems. Disturbance may limit competition and niche differentiation, which are frequently posited to underlie BEFRs. We provide the first exploration of the relationship between tree species diversity and biomass, one measure of ecosystem function, across southern African woodlands and savannas, an ecological system rife with disturbance from fire, herbivores and humans. We used > 1000 vegetation plots distributed across 10 southern African countries and structural equation modelling to determine the relationship between tree species diversity and above-ground woody biomass, accounting for interacting effects of resource availability, disturbance by fire, tree stem density and vegetation type. We found positive effects of tree species diversity on above-ground biomass, operating via increased structural diversity. The observed BEFR was highly dependent on organismal density, with a minimum threshold of c. 180 mature stems ha-1 . We found that water availability mainly affects biomass indirectly, via increasing species diversity. The study underlines the close association between tree diversity, ecosystem structure, environment and function in highly disturbed savannas and woodlands. We suggest that tree diversity is an under-appreciated determinant of wooded ecosystem structure and function.

Reproductive character displacement and potential underlying drivers in a species-rich and florally diverse lineage of tropical angiosperms (Ruellia; Acanthaceae).

Reproductive character displacement is a pattern whereby sympatric lineages diverge more in reproductive character morphology than allopatric lineages. This pattern has been observed in many plant species, but comparably few have sought to disentangle underlying mechanisms. Here, in a diverse lineage of Neotropical plants (Ruellia; Acanthaceae), we present evidence of reproductive character displacement in a macroevolutionary framework (i.e., among species) and document mechanistic underpinnings. In a series of interspecific hand pollinations in a controlled glasshouse environment, we found that crosses between species that differed more in overall flower size, particularly in style length, were significantly less likely to produce viable seeds. Further, species pairs that failed to set seed were more likely to have sympatric distributions in nature. Competition for pollinators and reinforcement to avoid costly interspecific mating could both result in these patterns and are not mutually exclusive processes. Our results add to growing evidence that reproductive character displacement contributes to exceptional floral diversity of angiosperms.

Amazon tree dominance across forest strata.

The forests of Amazonia are among the most biodiverse plant communities on Earth. Given the immediate threats posed by climate and land-use change, an improved understanding of how this extraordinary biodiversity is spatially organized is urgently required to develop effective conservation strategies. Most Amazonian tree species are extremely rare but a few are common across the region. Indeed, just 227 'hyperdominant' species account for >50% of all individuals >10 cm diameter at 1.3 m in height. Yet, the degree to which the phenomenon of hyperdominance is sensitive to tree size, the extent to which the composition of dominant species changes with size class and how evolutionary history constrains tree hyperdominance, all remain unknown. Here, we use a large floristic dataset to show that, while hyperdominance is a universal phenomenon across forest strata, different species dominate the forest understory, midstory and canopy. We further find that, although species belonging to a range of phylogenetically dispersed lineages have become hyperdominant in small size classes, hyperdominants in large size classes are restricted to a few lineages. Our results demonstrate that it is essential to consider all forest strata to understand regional patterns of dominance and composition in Amazonia. More generally, through the lens of 654 hyperdominant species, we outline a tractable pathway for understanding the functioning of half of Amazonian forests across vertical strata and geographical locations.

Adaptation and coordinated evolution of plant hydraulic traits.

Hydraulic properties control plant responses to climate and are likely to be under strong selective pressure, but their macro-evolutionary history remains poorly characterised. To fill this gap, we compiled a global dataset of hydraulic traits describing xylem conductivity (Ks ), xylem resistance to embolism (P50), sapwood allocation relative to leaf area (Hv) and drought exposure (ψmin ), and matched it with global seed plant phylogenies. Individually, these traits present medium to high levels of phylogenetic signal, partly related to environmental selective pressures shaping lineage evolution. Most of these traits evolved independently of each other, being co-selected by the same environmental pressures. However, the evolutionary correlations between P50 and ψmin and between Ks and Hv show signs of deeper evolutionary integration because of functional, developmental or genetic constraints, conforming to evolutionary modules. We do not detect evolutionary integration between conductivity and resistance to embolism, rejecting a hardwired trade-off for this pair of traits.

Freezing and water availability structure the evolutionary diversity of trees across the Americas.

The historical course of evolutionary diversification shapes the current distribution of biodiversity, but the main forces constraining diversification are still a subject of debate. We unveil the evolutionary structure of tree species assemblages across the Americas to assess whether an inability to move or an inability to evolve is the predominant constraint in plant diversification and biogeography. We find a fundamental divide in tree lineage composition between tropical and extratropical environments, defined by the absence versus presence of freezing temperatures. Within the Neotropics, we uncover a further evolutionary split between moist and dry forests. Our results demonstrate that American tree lineages tend to retain their ancestral environmental relationships and that phylogenetic niche conservatism is the primary force structuring the distribution of tree biodiversity. Our study establishes the pervasive importance of niche conservatism to community assembly even at intercontinental scales.

Evolutionary diversity in tropical tree communities peaks at intermediate precipitation.

Global patterns of species and evolutionary diversity in plants are primarily determined by a temperature gradient, but precipitation gradients may be more important within the tropics, where plant species richness is positively associated with the amount of rainfall. The impact of precipitation on the distribution of evolutionary diversity, however, is largely unexplored. Here we detail how evolutionary diversity varies along precipitation gradients by bringing together a comprehensive database on the composition of angiosperm tree communities across lowland tropical South America (2,025 inventories from wet to arid biomes), and a new, large-scale phylogenetic hypothesis for the genera that occur in these ecosystems. We find a marked reduction in the evolutionary diversity of communities at low precipitation. However, unlike species richness, evolutionary diversity does not continually increase with rainfall. Rather, our results show that the greatest evolutionary diversity is found in intermediate precipitation regimes, and that there is a decline in evolutionary diversity above 1,490 mm of mean annual rainfall. If conservation is to prioritise evolutionary diversity, areas of intermediate precipitation that are found in the South American 'arc of deforestation', but which have been neglected in the design of protected area networks in the tropics, merit increased conservation attention.

Evolutionary diversity is associated with wood productivity in Amazonian forests.

Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative importance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: aboveground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that additional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical forest communities with more distantly related taxa have greater wood productivity.

Comparative phylogeography of five widespread tree species: Insights into the history of western Amazonia.

Various historical processes have been put forth as drivers of patterns in the spatial distribution of Amazonian trees and their population genetic variation. We tested whether five widespread tree species show congruent phylogeographic breaks and similar patterns of demographic expansion, which could be related to proposed Pleistocene refugia or the presence of geological arches in western Amazonia. We sampled Otoba parvifolia/glycycarpa (Myristicaceae), Clarisia biflora, Poulsenia armata, Ficus insipida (all Moraceae), and Jacaratia digitata (Caricaceae) across the western Amazon Basin. Plastid DNA (trnH-psbA; 674 individuals from 34 populations) and nuclear ribosomal internal transcribed spacers (ITS; 214 individuals from 30 populations) were sequenced to assess genetic diversity, genetic differentiation, population genetic structure, and demographic patterns. Overall genetic diversity for both markers varied among species, with higher values in populations of shade-tolerant species than in pioneer species. Spatial analysis of molecular variance (SAMOVA) identified three genetically differentiated groups for the plastid marker for each species, but the areas of genetic differentiation were not concordant among species. Fewer SAMOVA groups were found for ITS, with no detectable genetic differentiation among populations in pioneers. The lack of spatially congruent phylogeographic breaks across species suggests no common biogeographic history of these Amazonian tree species. The idiosyncratic phylogeographic patterns of species could be due instead to species-specific responses to geological and climatic changes. Population genetic patterns were similar among species with similar biological features, indicating that the ecological characteristics of species impact large-scale phylogeography.

Drought-induced mortality in Scots pine: opening the metabolic black box.

Forests are sensitive to droughts, which increase the mortality rate of tree species. Various processes have been proposed to underlie drought-induced tree mortality, including hydraulic failure, carbon starvation and increased susceptibility to natural enemies. To give insights into these processes, we assessed the metabolic effects of a mortality-inducing drought on seedlings of Pinus sylvestris L. (Scots Pine), a widespread and important Eurasian species. We found divergence over time in the foliar metabolic composition of droughted vs well-watered seedlings, with the former showing increased abundance of aromatic amino acids and decreases in secondary metabolism associated with defence. We observed no significant differences amongst provenances in these effects: seedlings from drought-prone areas showed the same foliar metabolic changes under drought as seedlings from moist environments, although morphological effects of drought varied by provenance. Overall, our results demonstrate how severe drought prior to death may target particular primary and secondary metabolic pathways, weakening defences against natural enemies and contributing to the risk of drought-induced mortality in P. sylvestris.

Compositional response of Amazon forests to climate change.

Most of the planet's diversity is concentrated in the tropics, which includes many regions undergoing rapid climate change. Yet, while climate-induced biodiversity changes are widely documented elsewhere, few studies have addressed this issue for lowland tropical ecosystems. Here we investigate whether the floristic and functional composition of intact lowland Amazonian forests have been changing by evaluating records from 106 long-term inventory plots spanning 30 years. We analyse three traits that have been hypothesized to respond to different environmental drivers (increase in moisture stress and atmospheric CO2 concentrations): maximum tree size, biogeographic water-deficit affiliation and wood density. Tree communities have become increasingly dominated by large-statured taxa, but to date there has been no detectable change in mean wood density or water deficit affiliation at the community level, despite most forest plots having experienced an intensification of the dry season. However, among newly recruited trees, dry-affiliated genera have become more abundant, while the mortality of wet-affiliated genera has increased in those plots where the dry season has intensified most. Thus, a slow shift to a more dry-affiliated Amazonia is underway, with changes in compositional dynamics (recruits and mortality) consistent with climate-change drivers, but yet to significantly impact whole-community composition. The Amazon observational record suggests that the increase in atmospheric CO2 is driving a shift within tree communities to large-statured species and that climate changes to date will impact forest composition, but long generation times of tropical trees mean that biodiversity change is lagging behind climate change.

Tracking of Host Defenses and Phylogeny During the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; Argidae).

Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their Inga hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their Inga hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with Inga is better correlated with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in Inga diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.

The long-term ecology and evolution of marine reptiles in a Jurassic seaway.

Marine reptiles flourished in the Mesozoic oceans, filling ecological roles today dominated by crocodylians, large fish, sharks and cetaceans. Many groups of these reptiles coexisted for over 50 million years (Myr), through major environmental changes. However, little is known about how the structure of their ecosystems or their ecologies changed over millions of years. We use the most common marine reptile fossils-teeth-to establish a quantitative system that assigns species to dietary guilds and then track the evolution of these guilds over the roughly 18-million-year history of a single seaway, the Jurassic Sub-Boreal Seaway of the United Kingdom. Groups did not significantly overlap in guild space, indicating that dietary niche partitioning enabled many species to live together. Although a highly diverse fauna was present throughout the history of the seaway, fish and squid eaters with piercing teeth declined over time while hard-object and large-prey specialists diversified, in concert with rising sea levels. High niche partitioning and spatial variation in dietary ecology related to sea depth also characterize modern marine tetrapod faunas, indicating a conserved ecological structure of the world's oceans that has persisted for over 150 Myr.

Chemocoding as an identification tool where morphological- and DNA-based methods fall short: Inga as a case study.

The need for species identification and taxonomic discovery has led to the development of innovative technologies for large-scale plant identification. DNA barcoding has been useful, but fails to distinguish among many species in species-rich plant genera, particularly in tropical regions. Here, we show that chemical fingerprinting, or 'chemocoding', has great potential for plant identification in challenging tropical biomes. Using untargeted metabolomics in combination with multivariate analysis, we constructed species-level fingerprints, which we define as chemocoding. We evaluated the utility of chemocoding with species that were defined morphologically and subject to next-generation DNA sequencing in the diverse and recently radiated neotropical genus Inga (Leguminosae), both at single study sites and across broad geographic scales. Our results show that chemocoding is a robust method for distinguishing morphologically similar species at a single site and for identifying widespread species across continental-scale ranges. Given that species are the fundamental unit of analysis for conservation and biodiversity research, the development of accurate identification methods is essential. We suggest that chemocoding will be a valuable additional source of data for a quick identification of plants, especially for groups where other methods fall short.

Aboveground Carbon Storage and Its Links to Stand Structure, Tree Diversity and Floristic Composition in South-Eastern Tanzania.

African savannas and dry forests represent a large, but poorly quantified store of biomass carbon and biodiversity. Improving this information is hindered by a lack of recent forest inventories, which are necessary for calibrating earth observation data and for evaluating the relationship between carbon stocks and tree diversity in the context of forest conservation (for example, REDD+). Here, we present new inventory data from south-eastern Tanzania, comprising more than 15,000 trees at 25 locations located across a gradient of aboveground woody carbon (AGC) stocks. We find that larger trees disproportionately contribute to AGC, with the largest 3.7% of individuals containing half the carbon. Tree species diversity and carbon stocks were positively related, implying a potential functional relationship between the two, and a 'win-win' scenario for conservation; however, lower biomass areas also contain diverse species assemblages meaning that carbon-oriented conservation may miss important areas of biodiversity. Despite these variations, we find that total tree abundance and biomass is skewed towards a few locally dominant species, with eight and nine species (5.7% of the total) accounting for over half the total measured trees and carbon, respectively. This finding implies that carbon production in these areas is channelled through a small number of relatively abundant species. Our results provide key insights into the structure and functioning of these heterogeneous ecosystems and indicate the need for novel strategies for future measurement and monitoring of carbon stocks and biodiversity, including the use for larger plots to capture spatial variations in large tree density and AGC stocks, and to allow the calibration of earth observation data.