My research investigates the origin and maintenance of Amazonian rain forest tree diversity. I am especially interested in the role that biotic interactions and environmental heterogeneity play in the morphological, functional, and genetic diversity of tropical trees, and how these factors influence the distribution and speciation of plants. An ideal study system is the endemic flora found on the many white-sand forests that are widely dispersed in patches throughout the Amazon basin. These ancient white-sand deposits constitute habitat islands, surrounded by other terra firme forests on more fertile soils that harbor edaphic-specialist tree species that are often closely related to their congeners on neighboring soil types. The main thrust of my research is to understand the evolution and maintenance of edaphic specialization by trees to these divergent soil types, and the role of herbivores in this process.

Current projects:

Habitat specialization and community assembly of Amazonian tree lineages

   Tropical forests are the most biodiverse areas on earth, whether measured at local or regional scales. An important component of regional diversity is beta diversity, the turnover of species composition between habitats. In the lowland Amazon, there exists substantial turnover in species composition among terra firme, flooded and white-sand forests. The predominant explanation for such habitat specialization invokes allocation-based tradeoffs in response to different biotic (herbivores and/or pathogens) and abiotic (nutrient limitation and drought stress) selection pressures. While experimental evidence suggests that habitat specialization can be well explained by these tradeoffs, these insights remain to be integrated with large-scale distributional data and phylogenetic data. Together with two collaborators, I was awarded an NSF grant in Ecology (2008-2011) to address the evolution of habitat specialization within five widespread Amazonian tree lineages at two areas on opposite sides of the Amazon basin. We have installed 80 plots in white sand, terra firme and flooded forest in Peru and French Guiana to test for patterns of habitat specialization within each country. We have found strong patterns of aboveground biomass differences between white-sand, terra firme and flooded forests in Peru and French Guiana (Baraloto et al. 2011, Global Change Biology). We are constructing molecular phylogenies for the regional species pool of each of the five lineages to test for phylogenetic clustering (closely-related taxa are more likely to co-occur) or overdispersion (closely-related taxa are less likely to co-occur) at different taxonomic and spatial scales.

     We are evaluating the contributions of abiotic and biotic mechanisms of performance tradeoffs by quantifying traits that confer flood tolerance, nutrient use efficiency, and chemical defense by using a reciprocal transplant experiment including habitat generalists and specialists from each of the five lineages. Reciprocal transplant experiments with twenty species each have been running in French Guiana and in Peru since 2009.  DNA extraction, PCR and sequencing of the trees collected in the inventory plots was completed in summer 2011.  Preliminary results are showing that species from the tree lineages are in general  demonstrating strong habitat associations (Lamarre et al. in review, Ecology).   We have measured soil characteristics and many physiological plant traits at the different habitat types and are finding evidence consistent with discrete and divergent plant strategies being favored in each habitat type (Fortunel et al. in review, Functional Ecology). The results from all of this work will shed light on the extent to which ecological tradeoffs in functional traits related to herbivore defense and physiological stress tolerance can explain the distribution of closely-related species.  At the same time, we will be providing a powerful test of the relative strength of the processes that determine community assembly and yield insight into the role that beta-diversity plays in the generation and maintenance of high overall tropical diversity.

The Anacardiaceae and Burseraceae: a comparative phylogenetic study

     The sister plant lineages Anacardiaceae and Burseraceae are ecologically and economically important, taxonomically problematic, and evolutionarily fascinating.  The two families each contain

approximately 750 species and are of the same age, but exhibit vastly different patterns of distribution and morphological diversification.  Their divergent characteristics provide an excellent opportunity to investigate the interaction of morphology, habitat, and species diversification. Together with four collaborators, I have been awarded a NSF-grant  in Systematics and Biological Inventories (2009-2012) that proposes to elucidate the phylogeny of the Anacardiaceae-Burseraceae lineage, resolving infrafamilial classification and generic delimitation.

     In my lab, we are working hard to compile the samples of the almost 200 species of Protium, Tetragastris and Crepidospermum (the tribe Protieae) from the Neotropics and the Old World tropics to reconstruct as comprehensive a phylogeny as possible. As of Summer 2011 we have DNA sequenced for more than 80% of the species from this group, and hope to publish a new phylogeny by the end of the year.  Moreover, we will use this phylogeny to investigate the role of morphological diversification, ecological specialization, and biogeographic history in species diversification.  We will use the molecular phylogenies generated in this study to elucidate whether the evolution of morphological diversity in reproductive structures is related to evolutionary shifts to new habitats or new continents.  In addition, phylogenetic, biogeographic, and paleobotanical data will be integrated to evaluate the relative importance of key innovations versus biogeographic factors such as time and area as drivers of species radiations in the Anacardiaceae and Burseraceae.

 

Environmental gradients and speciation

      My phylogenetic results with the tropical family Burseraceae supports the hypothesis that edaphic heterogeneity can drive parapatric speciation, i.e. steep environmental gradients allow for evolutionary divergence in the presence of limited gene flow. There are five species of Protium white sand specialists in the Peruvian Amazon, and my data indicate that white-sand specialization evolved at least five times independently in the genus.  Four of these white-sand specialists belong to a complex of subspecies or varieties that include clay specialists in the same geographic area. These four sister pairs have widespread distributions across the white sand and clay forests of the entire Amazon basin and therefore will permit a rigorous test of the role of environmental gradients in the process of lineage diversification.  The most widespread and common of these is Protium subserratum, the focus of many of my lab’s current research projects to understand habitat specialization in tropical trees.

     First, I am reconstructing the genealogical relationships of  populations from both white-sand forest and terra firme (brown sand and clay) of Protium subserratum Engl. and its close relatives using chloroplast and single-copy nuclear DNA markers from the hundreds of trees that I have collected with colleagues and georeferenced from multiple sites in the Peruvian Amazon, Brazilian Amazon, Guyana, and French Guiana.. Protium subserratum is a morphologically variable taxon that has several different morphotypes, (some linked to soil type) and it is sister to two white-sand specialists, one of which is a new species Protium alvarezianum Daly and P. Fine that we recently  named due to its many unique molecular and morphological characters (Daly and Fine in press, Systematic Botany).  In addition, we have found that edaphic specialization has evolved multiple times just within Protium subserratum (Fine et al. in press, Journal of Biogeography) and that soil type is a much more important factor than distance structuring phylogeographic patterns, consistent with the predictions of ecological speciation. Next, field and laboratory studies of physiological traits such as nutrient use efficiency, drought tolerance, and anti-herbivore defense will permit us to identify the functional traits requisite for specialization onto a given soil type. In 2008, I began a new reciprocal transplant experiment with seeds collected from multiple populations of the Peruvian clay and sand specialist trees in my genetic study.  Finally, together with my graduate student, Tracy Misiewicz, we are currently developing a microsatellite library (funded by the Vincent Coates fund) for Protium subserratum to quantify the level of gene flow (if any) between white sand and clay lineages. If functional traits are divergent even in the face of gene flow between white sand and clay populations, this may mean we are catching ecotonal speciation in action; that even the stabilizing effect of gene flow is not enough to overwhelm the selective advantages of local adaptation to soil type.

Phylogenies, species turnover, and community assembly

       One of my main big-picture interests is to understand the importance of phylogenetic history in shaping ecological community composition.  To this end, I have worked on two conceptual projects to integrate phylogenetics into ecological studies.  First, with Catherine Graham, I published a conceptual paper called “Phylogenetic beta diversity:  linking ecological and evolutionary processes across space in time” which explores the utility of integrating phylogenetic data into studies of species turnover (Graham and Fine 2008, Ecology Letters).  Our paper makes some conceptual advances regarding the predictions of what patterns of community relatedness might be present at different spatial scales, different habitat types, and depending on the extent of niche conservatism in a given lineage. We explore how these new metrics can improve our understanding of the mechanisms underlying community assembly (speciation, dispersal, and environmental filtering). Second, I participated in a wide-ranging review paper called “The merging of community ecology and phylogenetic biology” (Cavender-Bares, Kozak, Fine and Kembel 2009, Ecology Letters). This paper reviews the entire history of applying phylogenetic thinking to questions in community ecology, theoretical considerations, methodologies, as well as current and future applications of this emerging discipline. Applying these new methods to Amazonian forests with our white-sand and terra firme plot database (Fine et al. 2010, Annals of the Missouri Botanical Garden), I have worked with a colleague, Steve Kembel to publish a paper that explores to what extent phylogenetic data gives insight into the relative importance of dispersal limitation, habitat specialization, and speciation in western Amazonian forests (Fine and Kembel, 2011, Ecography).

 

The role of plant-insect interactions in the evolution of chemical defense and lineage diversification in Amazonian forests

      Biologists have long proposed that plant and insect diversity are directly related, however, substantial tests of the patterns and mechanisms relating plant chemical defense to speciation in plants or insects remains to be directly investigated. With the help of the Hellman Family Foundation, I have begun an integrative study uniting functional and genetic bases underlying plant defense chemistry with species-level phylogenies of both tropical trees and herbivorous insects. We will  compare the timing and congruence of plant and herbivore species radiations and integrate this with functional and genomic studies of chemical defenses that putatively mediate these coevolutionary interactions.

      We are pursuing these questions both at the level of the genus Protium as well as among populations of a single species. To date, we have used Protium subserratum (described above under “Speciation Across Ecological Gradients”) as a model system to characterize defensive chemistry, insect herbivore assemblages and functional genes underlying terpene defense.  Preliminary results are consistent with the geographic mosaic hypothesis – individuals within populations share similar chemical profiles and there are quantitative differences in chemical compounds among populations as well as different insect herbivore assemblages in white-sand versus clay forest habitats as well as between French Guianan and Peruvian populations. This work is in preparation for submission in Fall 2011 (Fine, Lokvam and Baraloto, in prep.).

      Meanwhile, a postdoctoral fellow in my lab, Felipe Zapata, has been taking the lead on studying the molecular evolution of terpene synthase genes in the genus Protium. For a set of species from across the Protium phylogeny, we have characterized terpene chemical profiles and variation in monoterpene synthases (TPSb), the genes controlling a fundamental step in monoterpene biosynthesis.  Preliminary analyses reveal i) considerable interspecific variation in composition and concentration of leaf terpenes, ii) evidence for excess of nonsynonymous substitutions on TPSb genes concentrated in few codons, and iii) variable selection levels along the TPSb phylogeny, with support for positive selection along few branches representing different species or speciation events.  These results were presented at the Botany meetings in July 2011, and will be submitted for publication later this fall.

Past Research

   My dissertation work addressed the processes responsible for the turnover in tree species compositions on different soil types in the Western Amazon. I performed a phylogenetically controlled reciprocal transplant experiment with 20 species from six tree genera in nutrient-poor white sand forests and nutrient-rich clay forests. I manipulated the presence of herbivores to see if the evolutionary tradeoff between defense investment and growth rate could explain the maintenance of habitat specialization. The results were clear: there were significant differences in growth rate and survival indicating that habitat specialization in these forests cannot be explained by soil factors alone. Clay specialist species outperformed white-sand specialists in both soil types when protected from herbivores. However, when unprotected, white-sand specialists dominated in white-sand forests and clay specialists dominated in clay forests. Herbivores, by preferentially attacking clay forest plants in white sand soils, sharpen habitat boundaries and increase the potential for habitat specialization in plants (Fine et al. 2004, Science). In addition, white-sand and clay specialists exhibited a growth-defense tradeoff; functional traits associated with white-sand or clay specialization were not plastic responses to different soil types, but instead fixed traits shaped by natural selection that have evolved repeatedly by convergent evolution. This fundamental tradeoff, mediated by herbivores, represents an important mechanism of plant coexistence that has been largely overlooked in studies of plant habitat specialization and niche assembly (Fine et al. 2006, Ecology). 

         Could the tradeoffs for growth and defense that we found in our transplant experiment be a mechanism that promotes habitat-mediated speciation? For a phylogenetic study of habitat specialization, I chose one monophyletic group of common and diverse tropical trees, the tribe Protieae (Crepidospermum, Protium, and Tetragastris of the Burseraceae) that included species that were found in white-sand, brown-sand, and clay soil types. In six locations spanning hundreds of kilometers across the Peruvian Amazon, we located more than 2000 individuals of ca. 40 species from the tribe Protieae, and found that almost 75% of the species were associated with only one soil type; either clay, brown sand or white sand, and these patterns were consistent throughout the entire Western Amazon. I reconstructed a molecular-based phylogeny of these trees using two nuclear ribosomal genes. I found that white sand specialization has evolved multiple times in the group, and that the closest relatives of white-sand specialists were always specialists of other soil types, consistent with the idea that ecological specialization is important in the diversification of this important lineage of Amazonian trees (Fine et al. 2005, Evolution).

          To see if the pervasive patterns of edaphic specialization that we found in the Burseraceae were common to the community of white-sand forest trees, we conducted extensive inventories of more than 3300 trees in six white-sand forests throughout the northern Peruvian Amazon, as well as in the neighboring forest types (clay and brown-sand soils) (Fine et al. in press, Folia Amazonica, Fine et al., in prep.). We found more than 100 species of trees that were endemic to white-sand forests, including many species that are either new to science or new collections for Peru.