Search

The lowland Amazon rainforest houses some of the greatest tree diversity on Earth. While the vast majority of these species are rare, a small number are common and widespread and thus considered to play a disproportionate role in many of the global ecosystem services provided by the Amazon. However, the extent to which dominant Amazonian tree species actually include multiple clades, each on their own unique evolutionary trajectory, is unknown. Here we investigate the extent to which lineage divergence may be occurring within Protium subserratum (Burseraceae), a common and widespread tree species that is monophyletic with populations exhibiting genotypic and phenotypic differences associated with soil and geography. Utilizing a combination of phylogenomic and population genomic methods with sampling from across the range, we found that P. subserratum contains at least eight distinct clades. Specialization onto white-sand soils has evolved independently at least twice within the species; however, phenotype is not correlated with soil type. Finally, cryptic diversity at the base of the Andes is associated with elevational shifts. Together these results lend support to the hypothesis that common and widespread Amazon tree species may not represent evolutionary cohesive units. Instead, these dominant species may more commonly represent species complexes, undergoing evolutionary transitions on a trajectory to become multiple range-restricted, specialist species., (© 2023 John Wiley & Sons Ltd.)

Recent studies have leveraged large datasets from plot-inventory networks to report a phenomenon of hyperdominance in Amazonian tree communities, concluding that few species are common and many are rare. However, taxonomic hypotheses may not be consistent across these large plot networks, potentially masking cryptic diversity and threatened rare taxa. In the current study, we have reviewed one of the most abundant putatively hyperdominant taxa, Protium heptaphyllum (Aubl.) Marchand (Burseraceae), long considered to be a taxonomically difficult species complex. Using morphological, genomic, and functional data, we present evidence that P. heptaphyllum sensu lato may represent eight separately evolving lineages, each warranting species status. Most of these lineages are geographically restricted, and few if any of them could be considered hyperdominant on their own. In addition, functional trait data are consistent with the hypothesis that trees from each lineage are adapted to distinct soil and climate conditions. Moreover, some of the newly discovered species are rare, with habitats currently experiencing rapid deforestation. We highlight an urgent need to improve sampling and methods for species discovery in order to avoid oversimplified assumptions regarding diversity and rarity in the tropics and the implications for ecosystem functioning and conservation.

Plants in the Burseraceae are globally recognized for producing resins and essential oils with medicinal properties and have economic value. In addition, most of the aromatic and non-aromatic components of Burseraceae resins are derived from a variety of terpene and terpenoid chemicals. Although terpene genes have been identified in model plant crops (e.g., Citrus , Arabidopsis ), very few genomic resources are available for non-model groups, including the highly diverse Burseraceae family. Here we report the assembly of a leaf transcriptome of Protium copal , an aromatic tree that has a large distribution in Central America, describe the functional annotation of putative terpene biosynthetic genes and compare terpene biosynthetic genes found in P. copal with those identified in other Burseraceae taxa. The genomic resources of Protium copal can be used to generate novel sequencing markers for population genetics and comparative phylogenetic studies, and to investigate the diversity and evolution of terpene genes in the Burseraceae.

Plant secondary metabolites play important ecological and evolutionary roles, most notably in the deterrence of natural enemies. The classical theory explaining the evolution of plant chemical diversity is that new defences arise through a pairwise co-evolutionary arms race between plants and their specialized natural enemies. However, plant species are bombarded by dozens of different herbivore taxa from disparate phylogenetic lineages that span a wide range of feeding strategies and have distinctive physiological constraints that interact differently with particular plant metabolites. How do plant defence chemicals evolve under such multiple and potentially contrasting selective pressures imposed by diverse herbivore communities? To tackle this question, we exhaustively characterized the chemical diversity and insect herbivore fauna from 31 sympatric species of Amazonian Protieae (Burseraceae) trees. Using a combination of phylogenetic, metabolomic and statistical learning tools, we show that secondary metabolites that were associated with repelling herbivores (1) were more frequent across the Protieae phylogeny and (2) were found in average higher abundance than other compounds. Our findings suggest that generalist herbivores can play an important role in shaping plant chemical diversity and support the hypothesis that chemical diversity can also arise from the cumulative outcome of multiple diffuse interactions.

Andean uplift and the collision of North and South America are thought to have major implications for the diversification of the Neotropical biota. However, few studies have investigated how these geological events may have influenced diversification. We present a multilocus phylogeny of 102 Protieae taxa (73% of published species), sampled pantropically, to test hypotheses about the relative importance of dispersal, vicariance, habitat specialization, and biotic factors in the diversification of this ecologically dominant tribe of Neotropical trees. Bayesian fossil-calibrated analyses date the Protieae stem at 55 Mya. Biogeographic analyses reconstruct an initial late Oligocene/early Miocene radiation in Amazonia for Neotropical Protieae, with several subsequent late Miocene dispersal events to Central America, the Caribbean, Brazil's Atlantic Forest, and the Chocó. Regional phylogenetic structure results indicate frequent dispersal among regions throughout the Miocene and many instances of more recent regional in situ speciation. Habitat specialization to white sand or flooded soils was common, especially in Amazonia. There was one significant increase in diversification rate coincident with colonization of the Neotropics, followed by a gradual decrease consistent with models of diversity-dependent cladogenesis. Dispersal, biotic interactions, and habitat specialization are thus hypothesized to be the most important processes underlying the diversification of the Protieae., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

Soil heterogeneity is an important driver of divergent natural selection in plants. Neotropical forests have the highest tree diversity on earth, and frequently, soil specialist congeners are distributed parapatrically. While the role of edaphic heterogeneity in the origin and maintenance of tropical tree diversity is unknown, it has been posited that natural selection across the patchwork of soils in the Amazon rainforest is important in driving and maintaining tree diversity. We examined genetic and morphological differentiation among populations of the tropical tree Protium subserratum growing parapatrically on the mosaic of white-sand, brown-sand and clay soils found throughout western Amazonia. Nuclear microsatellites and leaf morphology were used to (i) quantify the extent of phenotypic and genetic divergence across habitat types, (ii) assess the importance of natural selection vs. drift in population divergence, (iii) determine the extent of hybridization and introgression across habitat types, (iv) estimate migration rates among populations. We found significant morphological variation correlated with soil type. Higher levels of genetic differentiation and lower migration rates were observed between adjacent populations found on different soil types than between geographically distant populations on the same soil type. PST -FST comparisons indicate a role for natural selection in population divergence among soil types. A small number of hybrids were detected suggesting that gene flow among soil specialist populations may occur at low frequencies. Our results suggest that edaphic specialization has occurred multiple times in P. subserratum and that divergent natural selection across edaphic boundaries may be a general mechanism promoting and maintaining Amazonian tree diversity., (© 2014 John Wiley & Sons Ltd.)

Herbivores are often implicated in the generation of the extraordinarily diverse tropical flora. One hypothesis linking enemies to plant diversification posits that the evolution of novel defenses allows plants to escape their enemies and expand their ranges. When range expansion involves entering a new habitat type, this could accelerate defense evolution if habitats contain different assemblages of herbivores and/or divergent resource availabilities that affect plant defense allocation. We evaluated this hypothesis by investigating two sister habitat specialist ecotypes of Protium subserratum (Burseraceae), a common Amazonian tree that occurs in white-sand and terra firme forests. We collected insect herbivores feeding on the plants, assessed whether growth differences between habitats were genetically based using a reciprocal transplant experiment, and sampled multiple populations of both lineages for defense chemistry. Protium subserratum plants were attacked mainly by chrysomelid beetles and cicadellid hemipterans. Assemblages of insect herbivores were dissimilar between populations of ecotypes from different habitats, as well as from the same habitat 100 km distant. Populations from terra firme habitats grew significantly faster than white-sand populations; they were taller, produced more leaf area, and had more chlorophyll. White-sand populations expressed more dry mass of secondary compounds and accumulated more flavone glycosides and oxidized terpenes, whereas terra firme populations produced a coumaroylquinic acid that was absent from white-sand populations. We interpret these results as strong evidence that herbivores and resource availability select for divergent types and amounts of defense investment in white-sand and terra firme lineages of Protium subserratum, which may contribute to habitat-mediated speciation in these trees.

The formation of spatial genetic structure (SGS) may originate from different patterns of seed deposition in the landscape, and is mostly determined by seed dispersal limitation. After dispersal, mechanisms such as filtering by environmental factors or attack by herbivores/pathogens throughout plant development stages, and potentially either disrupt or intensify SGS patterns. We investigated how the genotype of Protium subserratum (Burseraceae), a common tree species in the Ducke Reserve, Brazil, is distributed across the landscape. We used seven microsatellite markers to assess the SGS among plants at different life stages and in different environments. By quantifying the patterns of relatedness among plants of different sizes, we inferred the ontogenetic stage in which SGS changes occurred, and compared these effects across soil types. Relatedness among seedlings decreased when distance between seedlings increased, especially for the youngest seedlings. However, this trend was not continued by older plants, as relatedness values were higher among neighboring individuals of the juvenile and adult size class. Contrasting relatedness patterns between seedlings and larger individuals suggests a trade-off between the negative effects of being near closely-related adults (e.g. due to herbivore and pathogen attack) and the advantage of being in a site favorable to establishment. We also found that soil texture strongly influenced density-dependence patterns, as young seedlings in clay soils were more related to each other than were seedlings in bottomland sandy soils, suggesting that the mechanisms that create and maintain patterns of SGS within a population may interact with environmental heterogeneity.

Premise of the Study: The first microsatellite primers were developed for Protium subserratum, a widespread Amazonian tree, to investigate genetic differentiation between populations found on clay, brown-sand, and white-sand soils. •, Methods and Results: Seventeen primer pairs were identified from two individuals of P. subserratum found on white-sand and brown-sand soil types. Polymorphism was analyzed in 63 individuals from a total of three populations, each found on a different soil type. The primers amplified tetra-, tri-, and dinucleotide repeats with three to 24 alleles per locus. Excluding monomorphic loci, observed and expected heterozygosities ranged from 0 to 0.852 and 0.036 to 0.901, respectively. •, Conclusions: These new microsatellite markers will be useful in studies of genetic diversity, population differentiation, and gene flow across habitat types in P. subserratum.

Protium subserratum (Burseraceae) is a neotropical tree species that is comprised of several habitat-specific ecotypes having distinct defense chemical profiles. A previously unknown triterpene, 25,30-dicarboxy-26,27,28,29-tetraacetoxy-10,11,14,15-tetrahydrosqualene, was isolated from P. subserratum young leaf tissue of one ecotype growing in Peru. The structure of 1 was determined by spectroscopic study, including 1 and 2D nuclear magnetic resonance experiments.

Environmental heterogeneity in the tropics is thought to lead to specialization in plants and thereby contribute to the diversity of the tropical flora. We examine this idea with data on the habitat specificity of 35 western Amazonian species from the genera Protium, Crepidospermum, and Tetragastris in the monophyletic tribe Protieae (Burseraceae) mapped on a molecular-based phylogeny. We surveyed three edaphic habitats that occur throughout terra firme Amazonia: white-sand, clay, and terrace soils in eight forests across more than 2000 km in the western Amazon. Twenty-six of the 35 species were found to be associated with only one of three soil types, and no species was associated with all three habitats; this pattern of edaphic specialization was consistent across the entire region. Habitat association mapped onto the phylogenetic tree shows association with terrace soils to be the probable ancestral state in the group, with subsequent speciation events onto clay and white-sand soils. The repeated gain of clay association within the clade likely coincides with the emergence of large areas of clay soils in the Miocene deposited during the Andean uplift. Character optimizations revealed that soil association was not phylogenetically clustered for white-sand and clay specialists, suggesting repeated independent evolution of soil specificity is common within the Protieae. This phylogenetic analysis also showed that multiple cases of putative sister taxa with parapatric distributions differ in their edaphic associations, suggesting that edaphic heterogeneity was an important driver of speciation in the Protieae in the Amazon basin.

Plant defense chemistry is often hypothesized to drive ecological and evolutionary success in diverse tropical forests, yet detailed characterizations of plant secondary metabolites in tropical plants are logistically challenging. Here, we explore a new integrative approach that combines visible‐to‐shortwave infrared (VSWIR) spectral reflectance data with detailed plant metabolomics data from 19 Protium (Burseraceae) tree species. Building on the discovery that different Protium species have unique chemistries yet share many secondary metabolites, we devised a method to test for associations between metabolites and VSWIR spectral data. Given species‐level variation in metabolite abundance, we correlated the concentration of particular chemicals with the reflectance of the spectral bands in a wavelength band per secondary metabolite matrix. We included 45 metabolites that were shared by at least 5 Protium species and correlated their per‐species foliar abundances against each one of 210 wavelength bands of field‐measured VSWIR spectra. Finally, we tested whether classes of similar metabolites showed similar relationships with spectral patterns. We found that many secondary metabolites yielded strong correlations with VSWIR spectra of Protium. Furthermore, important Protium metabolite classes such as procyanidins (condensed tannins) and phytosterols were grouped together in a hierarchical clustering analysis (Ward's algorithm), confirming similarity in their associations with plant spectral patterns. We also found a significant correlation in the phenolics content between juvenile and canopy trees of the same species, suggesting that species‐level variation in defense chemistry is consistent across life stages and geographic distribution. We conclude that the integration of spectral and metabolic approaches could represent a powerful and economical method to characterize important aspects of tropical plant defense chemistry. [ABSTRACT FROM AUTHOR]

Methods to quantify plant‐insect interactions in tropical forests may miss many important arthropods and can be time consuming and uneven in capture efficiency. We describe the Amazonas‐trap, a new method that rapidly envelops the target plant for sampling arthropods. We evaluated the efficiency of the Amazonas‐trap by comparing it with two commonly used sampling methods to collect arthropods from plants: the beating tray and manual collection. Samples were collected in 10 permanent plots, in the Ducke forest reserve, Manaus (Amazonas, Brazil). In each plot we sampled 18 plant individuals of Protium sp. (Burseraceae): six by a beating tray, six by manual collection, and six using the Amazonas‐trap. All insects were identified to the family level and those belonging to the order Hymenoptera were identified to the species and morphospecies level. The new method sampled more insect families and more Hymenoptera species than tree beating and manual collection. Of the 75 total families collected, 20 were sampled exclusively by the Amazonas‐trap, seven were only collected with a beating tray, and seven were sampled exclusively with manual collecting. A similar pattern was found for abundance: Amazonas‐trap sampled more individuals, followed by the beating tray and manual collection. Small and winged arthropods were more abundant in Amazonas‐trap, explaining the highest richness of Hymenoptera and insect families sampled with this method. The new method sampled more spiders, wood‐fungi feeders, sap suckers, omnivorous, parasitoids, and insect predators than the other methods, but was equally effective in sampling leaf‐feeders and ants. Amazonas‐trap was more time consuming in the field, but for all diversity parameters evaluated, the new method showed better performance for collecting invertebrates on plants. [ABSTRACT FROM AUTHOR]

Little is known about the mechanisms promoting or limiting the coexistence of functionally divergent species in hyperdiverse tropical tree genera. Density-dependent enemy attacks have been proposed to be a major driver for the local coexistence of chemically divergent congeneric species. At the same time, we expect local soil conditions to favor the coexistence of species sharing similar functional traits related to resource use strategies, while environmental heterogeneity would promote the diversity of these traits at both local and large spatial scales. To test how these traits mediate species coexistence, we used functional trait data for 29 species from the tree genus Protium (Burseraceae), collected in 19 plots (2 ha each) in the Peruvian Amazon. We characterized the presence-absence of 189 plant secondary metabolites (SM) for 27 of these species, and 14 functional traits associated with resource use strategies (RUT) for 16 species. Based on these data, we found that SM were significantly more dissimilar than null expectations for species co-occurring within plots, whereas RUT were significantly more similar. These results were consistent with the hypothesis that density-dependent enemy attacks contribute to the local coexistence of congeneric species displaying divergent chemical defenses, whereas local habitat conditions filter species with similar RUT. Using measurements of nine soil properties in each plot, we also found a significant turnover of RUT traits with increasing dissimilarity of soil texture and nutrient availabilities, providing support for the hypothesis that soil heterogeneity maintains functional diversity at larger spatial scales (from 500 m up to ca. 200 km) in Protium communities. Our study provides new evidence suggesting that density-dependent enemy attacks and soil heterogeneity both contribute to maintaining high species richness in diverse tropical forests. [ABSTRACT FROM AUTHOR]

Many angiosperm families are distributed pantropically, yet for any given continent little is known about which lineages are ancient residents or recent arrivals. Here we use a comprehensive sampling of the pantropical sister pair Anacardiaceae and Burseraceae to assess the relative importance of continental vicariance, long-distance dispersal and niche-conservatism in generating its distinctive pattern of diversity over time. Each family has approximately the same number of species and identical stem age, yet Anacardiaceae display a broader range of fruit morphologies and dispersal strategies and include species that can withstand freezing temperatures, whereas Burseraceae do not. We found that nuclear and chloroplast data yielded a highly supported phylogenetic reconstruction that supports current taxonomic concepts and time-calibrated biogeographic reconstructions that are broadly congruent with the fossil record. We conclude that the most recent common ancestor of these families was widespread and likely distributed in the Northern Hemisphere during the Cretaceous and that vicariance between Eastern and Western Hemispheres coincided with the initial divergence of the families. The tempo of diversification of the families is strikingly different. Anacardiaceae steadily accumulated lineages starting in the Late Cretaceous-Paleocene while the majority of Burseraceae diversification occurred in the Miocene. Multiple dispersal- and vicariance-based intercontinental colonization events are inferred for both families throughout the past 100 million years. However, Anacardiaceae have shifted climatic niches frequently during this time, while Burseraceae have experienced very few shifts between dry and wet climates and only in the tropics. Thus, we conclude that both Anacardiaceae and Burseraceae move easily but that Anacardiaceae have adapted more often, either due to more varied selective pressures or greater intrinsic lability. [ABSTRACT FROM AUTHOR]

Highlights: [•] There are three and potentially five TPSb genes copies within the Protium genome. [•] Most copies are evolving under relaxed and/or stabilizing selection. [•] Monoterpenes may be involved in signaling and physiological stress protection. [ABSTRACT FROM AUTHOR]

Aim Edaphic heterogeneity may be an important driver of population differentiation in the Amazon but remains to be investigated in trees. We compared the phylogeographic structure across the geographic distribution of two Protium (Burseraceae) species with different degrees of edaphic specialization: Protium alvarezianum, an edaphic specialist of white-sand habitat islands; and Protium subserratum, an edaphic generalist found in white sand as well as in more widespread soil types. We predicted that in the edaphic specialist, geographic distance would structure populations more strongly than in the edaphic generalist, and that soil type would not structure populations in the edaphic generalist unless habitat acts as a barrier promoting population differentiation. Location Tropical rain forests of the Peruvian and Brazilian Amazon, Guyana and French Guiana. Methods We sequenced 1209-1211 bp of non-coding nuclear ribosomal DNA (internal transcribed spacer and external transcribed spacer) and a neutral low-copy nuclear gene (phytochrome C) from P. subserratum ( n = 65, 10 populations) and P. alvarezianum ( n = 19, three populations). We conducted a Bayesian phylogenetic analysis, constructed maximum parsimony haplotype networks and assessed population differentiation among groups (soil type or geographic locality) using analysis of molecular variance and spatial analysis of molecular variance. Results The edaphic specialist exhibited considerable genetic differentiation among geographically distant populations. The edaphic generalist showed significant genetic differentiation between the Guianan and Amazon Basin populations. Within Peru, soil type and not geographic distance explained most of the variation among populations. Non-white-sand populations in Peru exhibited lower haplotype/nucleotide diversity than white-sand populations, were each other's close relatives, and formed an unresolved clade derived from within the white-sand populations. Main conclusions Geographic distance is a stronger driver of population differentiation in the edaphic specialist than in the generalist. However, this difference did not appear to be related to edaphic generalism per se as adjacent populations from both soil types in the edaphic generalist did not share many haplotypes. Populations of the edaphic generalist in white-sand habitats exhibited high haplotype diversity and shared haplotypes with distant white-sand habitat islands, indicating that they have either efficient long-distance dispersal and/or larger ancestral effective population sizes and thus retain ancestral polymorphisms. These results highlight the importance of edaphic heterogeneity in promoting population differentiation in tropical trees. [ABSTRACT FROM AUTHOR]

The article presents a study that describes protium section papilloprotium and protium alvarezianum and provides a key to the four species of the section. The study distinguishes the section based on its papilate abaxial surface, and the petals saccate at base and villous adaxially. It highlights the common ancestor shared by P. ferrugineum with two small clades.