Paul S. Manos - US grants

9707945 Manos The ecologically and economically important family Fagaceae of oaks, beeches, and chestnuts is most familiar to temperate-zone botanists from a relative handful of species. But the family has many tropical species, and is especially diverse in southeast Asia, where Dr. Paul Manos of Duke University will be conducting field work to sample the two largest genera, Castanopsis and Lithocarpus. These two genera comprise nearly half of the species diversity in the family and represent an even greater range of morphological diversity in the characteristic cupule (the burr or acorn) than found in the temperate-zone members of the family. One goal of the research is to infer genealogical or phylogenetic relationships among the many tropical species, by integrating traditional morphological knowledge of these plants with new molecular data from DNA sequencing of nuclear ribosomal genes, which provide a direct measure of mutational differences between samples. This phylogenetic framework in turn will allow analysis of the history of development of various cupule morphologies in the lineages of tropical and subtropical Fagaceae, especially among cupule types that are indistinguishable at maturity but suspected of convergent evolution from different juvenile stages. The range and history of species diversification in the "tropical chestnuts" or castaneoids are poorly known. Field work, study of existing herbarium collections, and new DNA sequence data will be brought together to improve our understanding of the basic taxonomy and phylogeny of these plants. Tropical diversity often contains key elements to understand the evolutionary history of plants in the temperate zone, and this is likely to be the case with the diverse, insect-pollinated Castanopsis and Lithocarpus of southeast Asia. The studies will prove useful in interpreting morphological evolution, and will place the major groups of castaneoids into a geographical as well as phylogenetic framework.

9972646
Manos and Arrington


Rockroses are ecologically important components of Northern Hemisphere


Mediterranean-type shrublands. The Iberian peninsula followed by the U.S. Atlantic Coastal Plain is particularly species-rich. Even though a diverse assortment of vegetative and floral features are present in the family, the Cistaceae are usually known for their aromatic, showy-flowered species which dominate Old World maquis (Corsican for rockrose) ecosystems. This is largely due to their
economic value to perfumery and horticulture, and their association with a spectacular parasitic flowering plant, Cytinus (family Rafflesiaceae), a root parasite whose only above-ground structure is its flowering stalk. The Cistaceae are promising candidates for studies geared toward a better
understanding of morphological form, breeding systems, chromosomal evolution, biogeography, shrubland ecology, and host-parasite relationships; however, research has been hindered by the lack of a reliable natural classification. The family has largely been neglected taxonomically, and higher- and lower-level taxonomy remain obscure because traditional schemes have revolved around "field identifiable" vegetative and floral attributes, with little agreement on their value in defining natural groups. In the past, prevailing ideas on what constitute primitive, specialized or convergent features have produced disparate opinions on cistalean relationships. This research by graduate student Jennifer Arrington, under the direction of Dr. Paul Manos at Duke University, represents the first phylogenetic approach to the classification of the Cistaceae and the first comprehensive taxonomic treatment since 1925.
In order to delimit taxa and develop a morphological matrix for evolutionary analyses, a close examination will be made of promising diagnostic traits of the flower such as the stigma, style, pollen and ovule, as well as chromosome number and developmental characteristics
pertaining to merosity (number of flower parts). Samples of all the known genera and of many of the described species have been or will soon be collected from throughout the native range of the family in North America and in Europe. This information will be supplemented by molecular genealogies based on chloroplast and nuclear DNA sequences, which will provide a comparative phylogenetic framework for research on morphological form, chromosomal evolution, host-specificity, and biogeography.

9972600
Manos and Jaramillo
Graduate student Alejandra Jaramillo, under the direction of Dr. Paul Manos at Duke University, is studying the taxonomic classification of the large genus Piper (the genus of black and white pepper, with ca. 1200 species) and the development of floral morphology in several species of this tropical group. Piper species occur as shrubs, lianas, and herbs in the understory and canopy of tropical forests worldwide. Although individual Piper flowers are minute, the species express a wide range of diversity in unisexual and bisexual forms, including various types of perfect flowers that differ in the number and positional relationships of their stamens. However, patterns of floral variation have not been independently tested as reliable indicators of phylogenetic (or genealogical) relationship. This project will emphasize the DNA sequencing of both nuclear and chloroplast genes as sources of evidence to construct a framework phylogeny for ca. 130 species representative of the subgenera and geographical diversity known for the genus, in order further to study ontogenetic (developmental) stages in flower morphology. Ontogenetic modifications, such as dioecy and extreme stamen reduction, will be mapped onto phylogenies to test the association between floral innovation and diversification across the genus. Phylogenetic analysis will also improve the subgeneric and sectional classification of this large genus, and help advance improved species-level delimitation. An improved understanding of the evolutionary history of Piper provides an opportunity to identify key floral innovations in the diversification of the largest genus of "primitive" dicots.

0073171
Clark
The range expansion by forest trees following rapid climatic warming during the early Holocene provides a useful analog for predicting the ability of trees to respond to future climate change. Currently, however, early Holocene migration rates determined from fossil pollen records can not be easily reconciled with models of seed dispersal. This dissertation research is an attempt to reconcile the historical record and the dispersal biology of common eastern deciduous forest trees. First, migration routes and glacial refugia based on the distribution of molecular markers (cpDNA haplotypes) throughout the modern range of Fagus grandifolia, Acer rubrum, and Quercus rubra will be reconstructed. Maps of Holocene range expansion based on molecular and pollen data will provide improved estimates of climate driven migration rates. This study will then evaluate the ability of seed dispersal models to account for these migration rates using a dispersal model developed by this research group. The model will be parameterized using the distribution of seedlings established in old-fields and closed forests. By integrating fossil pollen and molecular data, this study will develop a more complete record of historical change. Explaining that change in terms of dispersal biology will allow a mechanistic basis for evaluating future change.

The goals of this study are: 1) to infer the phylogeny, or set of genealogical relationships, of Hibbertia using chloroplast and nuclear DNA sequences; 2) to document the pattern of floral development using Scanning Electron Microscopy for selected Hibbertia species; 3) compare the sequences of developmental events between species in the context of a relativistic time course, so that developmental events may be compared without the assumption that similar appearing stages in the of different species represent units for direct comparison. The combination of data on the pattern formation and relative timing of organ development will then be analyzed in a phylogenetic context, so that hypotheses of how relative changes in the timing of developmental events have affected mature floral form may be explicitly tested. Preliminary data suggests that in one major group of Hibbertia, the timing of the origination of the carpels (female floral organs) has been advanced, relative to the initiation of stamens (male, pollen-producing floral organs), so that the carpels take up space on the lower half the floral meristem (aggregation of undifferentiated, embryonic cells) that in other taxa produce stamens. The result of relative timing shift is the transition of a radially symmetric patterning of stamens around the flower, to a bilaterally symmetric arrangement of stamens formed exclusively on the top half of the flower. This study will be among the first to elucidate the evolutionary processes behind differences in floral morphology at the level of the floral groundplan.


The study of floral morphological diversity stands as one of the principal foci of botanical research. While the implications of this field for flowering plant classification have been the most long-standing and far-reaching, the study of floral evolution impacts economically important disciplines such as horticulture and plant breeding. A group with particularly great potential to further our understanding of the evolution of floral form is Hibbertia (family Dilleniaceae), a genus of ca. 150 species distributed in Australia, New Caledonia, and Madagascar. What makes Hibbertia such an ideal candidate for such a study is, as put forth by the great evolutionary botanist G. L. Stebbins (1974), that "[t]here is probably no other genus of angiosperms that exhibits such a high degree of variation in those characteristics that are often regarded as 'fundamental' and are usually associated with the separation of genera or even higher categories."

Anticipated rapid climatic change over the next decades to centuries raises the concern that plant populations will be unable to migrate fast enough to track changing environmental conditions. Migration rates depend on dispersal of seed and on barriers to population spread, such as mountain ranges, large water bodies, and patterns of urban and agricultural land use. Range expansions at the end of the last ice age provide evidence that populations tracked global change in the past, but current evidence does not indicate the speed of these migrations. The proposed research will determine the pathways of past population spread and provide insights into rates of corresponding migrations. We will construct and analyze maps of chloroplast DNA variation across the ranges of common eastern North American tree species. Such maps reveal the "genetic fingerprint " of late-glacial refugia and post-glacial migration routes, and complement existing data for fossil pollen. The maps of post-glacial migration we will provide a framework for analysis of population expansion. Results will be used to test hypotheses concerning how growth of trees and dispersal of seeds affect the potential of plants to track rapid environmental change.

Dr. Paul Manos of Duke University is studying the predominantly paleotropical tree genus Lithocarpus (ca. 300 species) to better understand the biological significance of variation in fruit morphology and DNA sequences across a diverse landscape. Modifications of the common acorn-like fruit typically mark subgroups within the genus, but such changes appear to have evolved more than once. The study will explore new quantitative methods to characterize changes in fruit shape and compare and combine these data with DNA sequences to test whether certain fruit types have multiple origins. The widespread distribution of Lithocarpus on the continent of Asia and throughout the Malayan Archipelago also provides an excellent opportunity to pursue the genetics of plant demography using chloroplast DNA variation, a maternally inherited marker that tracks seed movement. By sampling individuals throughout the range of the genus, the study will address the relationship between plant migration and geological/paleoecological change. A variety of methods will be used to test explicit hypotheses of refugial areas and migration routes based on paleoecological data. Trees will be sampled to examine genealogical structure within populations through contrasting nuclear and cytoplasmic molecular markers with reference to taxonomy, geography, and differential patterns of genome evolution.
The study of organismal diversity and molecular evolution in tropical tree species requires a framework built upon thorough knowledge of natural history, taxonomy, morphology, and genealogical relationships. Species in the oak family present a broad spectrum of opportunities to study diversity in form and patterns of plant migration and gene flow. Tropical woody plants are poorly studied in this regard and a variety of basic biological questions have never been addressed in the ecologically important relatives of the oaks. Given the amount of carbon storage, ecosystem services, biodiversity, and physical structure provided to the tropical rainforest by this tree community, this study would be one of first of its kind to apply several powerful molecular techniques to an important tropical genus.

This research concerns a group of approximately 22 plant species that has diversified in the Sonoran and Chihuahuan Deserts, the genus Boerhavia. Species of Boerhavia can self-pollinate, and also have very different flower sizes, which affects how often insects visit and transfer pollen between plants. This project tests whether species with smaller flowers have a greater amount of genetic differentiation between populations that are highly inbred, because pollen can not frequently flow between populations. Genetic fingerprinting techniques will establish the proportion of seeds on a plant that are sired by other individuals. This will be done for many individuals per population, for all North American species. The same data will also provide estimates of the differences between populations, and their level of inbreeding. Combining this data with the evolutionary history of Boerhavia, it will be possible to test whether species with smaller flowers exhibit populations diverging into genetically distinct species.

This project will provide training for N. Douglas in botany and population biology. Mexican botanists are collaborating in this research. The project will estimate the total genetic diversity of four extremely rare, unprotected species in the U.S. and Mexico. Thus, it will find an audience among botanists, ecologists, and conservationists in both nations.

The Department of Biology at Duke University will host seven undergraduate students each summer in a research program in Bioinformatic and Phylogenetic Approaches to the Study of Plant and Fungal Biodiversity. The site is supported by the Department of Defense in partnership with the NSF REU program. Applications to participate in Bioinformatics and Phylogenetics will be accepted from sophomore and junior undergraduates. Students with limited opportunities for research, including under-represented minorities, are especially encouraged to apply. The seven faculty who will serve as mentors in our program have active research programs ranging from the Tree of Life initiative to reconstructing species-level genealogies, and within species and population-level genomic-based biology of plants and fungi. The focus of the ten-week summer program will be a research mentorship with a participating faculty member. The series will strive to reinforce the intellectual integration of the undergraduate participants with graduate students and senior personnel by developing the programmatic theme including three types of activities into a ten-week undergraduate research experience: (1) a two-day orientation; (2) a twice-weekly seminar/discussion series; and (3) a research forum for presenting the summer's results and conclusions. The intention is to provide a supportive environment to the students as they progress through the summer, as well as to reinforce the image of science as an interactive enterprise. Duke University has a history of successful undergraduate summer research programs, especially those that provide training experiences for women and minorities. We have drawn from this experience and will be able to make use of existing administrative structures both for recruiting candidates to the program and for providing the logistical support necessary for an engaging and stimulating research experience. The research environment at Duke offers state-of-the-art facilities, including world-class research collections of plants and fungi, a diverse living reference collection of plants and cultures of fungi and algae, the Duke Biology Genetic Analysis Facility, and the experimental setting provided by the Duke Forest, including the Forest-Atmosphere Carbon Transfer and Storage (FACTS-I) site. For further information and application materials, please contact Dr. Paul Manos at pmanos@duke.edu or (919) 660-7358, or visit http://www.biology.duke.edu/reu.

The flowering plant family Fagaceae (ca. 1000 species, including the beeches, oaks, and chestnuts) plays a major ecological role in several broadly distributed ecosystems of the Northern Hemisphere. Duke University researchers Paul Manos and Sang-Hun Oh propose to conduct a thorough evolutionary investigation of this remarkable diversification of woody species. Ideally, the study of the pattern and process of species diversification or speciation requires a robust estimate of species relationships, accurate knowledge of species numbers, and a rich fossil record. In the oak family (Fagaceae), these conditions are nearly in place, making it a premier group for the research proposed. Research completed to date establishes a robust platform to produce a genealogy of Fagaceae using several DNA regions, specifically alternative low-copy nuclear genes across 75 species. The resulting genealogy will be used to address long-standing classical questions regarding the evolution of reproductive structures and traits, and independently to assess traditionally described genera. A second goal requires the use of fossils to calibrate the evolutionary history of the family. Within this chronicle of evolution, hypotheses of key innovation or critical factors linked to increases in the speciation rate, will be tested using established methods that test for shifts in species richness. Measures of phylogenetic diversity or the amount of DNA variation also will be compared among groups to test for significant differences that may correlate with shifts in the rate of diversification. The proposed research aims to link several aspects of macroevolutionary analysis to produce an explicit account of this ecologically significant diversification. While the family Fagaceae is well-studied, the synthesis proposed here has not been attempted before, and its implications reach beyond systematic biology and into emerging investigations of the causes of diversification and its consequences to molecular and genealogical diversity.
The proposed research will integrate training at several levels. Dr. Sang-Hun Oh will train and benefit from a range of evolutionary activities present at Duke University. A graduate student will receive training in the methods proposed, and the research team will include two undergraduate students to be recruited through a Duke summer program funded through the NSF REU-Sites program. Proposed outreach activities include the development of a website dedicated to Fagaceae research at Duke, which will form the basis for an expanded contribution to the Tree of Life Project.

This project investigates how parasites invade and persist in host populations. The study's approach is historical and compares the post-glacial migration of a parasitic plant, Epifagus virginiana (beechdrop; Orobanchaceae), with its host, Fagus grandifolia (American beech; Fagaceae). The objectives are (A) to reconstruct the broad scale colonization patterns of E. virginiana using genetic data, (B) to investigate potential forces (e.g., host density effects, limited parasite dispersal) limiting parasite infection through fine scale mapping and genotyping, and (C) to test for local adaptation of the parasite through germination studies. This research will produce a comprehensive migration history of this parasite with an emphasis on what factors influenced its invasion, and it builds upon previous work on the host's colonization history.

Understanding what controls the spread of parasites is especially relevant today considering that future climate change may force species to move at their full migration capacities. The proposed study will provide significant data on herbaceous plant migration that is currently missing and can answer questions about the cohesiveness of communities during migration. Results from this study will be incorporated into interpretive signs along public nature trails that describe the natural history of the beech woods and parasitic plants.

The co-evolution of plants and their pollinators has given rise to a variety of flower shapes, colors, and sizes. Certain flower traits are frequently correlated, and these correlations define what is commonly termed a "pollination syndrome". For example, white flowers that open at night and have long tubes are generally indicative of hawkmoth pollination.

Transitions in pollination syndromes are widely believed to contribute to plant speciation, including the origin and radiation of the flowering plants. The goal of this research is to study such transitions by focusing on the species-rich genus Ruellia. With approximately 300 species, Ruellia is the second largest genus in the tropical family Acanthaceae (ca. 4,000 species). Based on preliminary evolutionary analyses (E. Tripp, unpub. data), closely related species often display a variety of pollination syndromes, indicating that pollinators have likely had a large role in the overall speciation of Ruellia. Though Mexico is a hotspot for Ruellia diversity, current taxonomic sampling and field collections of Mexican Ruellia species is poor. This proposal describes how a plant collecting expedition through southern portions of Mexico, coupled with museum-based work out of national and international herbaria, will permit a full exploration of species relationships and the evolution of pollination syndromes in Ruellia. Methods include molecular sequencing, standard genealogical analyses, plant identification and morphological analyses, field collections and herbarium curation, and the construction of local and/or regional floristic treatments.

Because pollination transitions contribute to plant diversification, studying such transitions as well as relationships among Ruellia species can lend insight into processes involved in plant speciation, and thus to the generation of biodiversity. Knowledge of biodiversity is of paramount importance to everyone, particularly knowledge of tropical taxa where critical habitat is disappearing at unprecedented rates. Further, botanical collections have been fundamental to all biological investigations and remain essential today, especially in tropical regions where much diversity has yet to be documented. It has been shown that collections data can be useful in conservation decision-making1,2. This work will benefit the conservation infrastructure in Mexico and promote international scientific collaboration between US and Mexican institutions, botanists, and students.

To ensure our success in understanding the history and future of biodiversity, it is imperative that the upcoming generation of biologists continue to be trained in traditional field biology and museum/herbarium curation, as well as modern molecular methods.

This study will improve understanding of the role that soil conditions play in plant diversification. Although soil conditions have long been seen as a key component of plant ecology, little is understood about the effect of soil conditions on plant evolution and diversification. The proposed research will use the plant genus Ceanothus as a model system for the study of how soil conditions affect diversification. Ceanothus contains a large number of species that are associated with unusual soils, and is thus an ideal setting in which to study the influence of soil conditions in diversification. The proposed research will use genetic data to determine evolutionary relationships among Ceanothus species. These data will then be combined with information on soil chemistry to infer the role that soil conditions have played in the diversification of Ceanothus.

The proposed research will take an interdisciplinary approach to understanding how soil conditions affect plant diversification, combining data and analytical methods from the disciplines of evolutionary biology, ecology, and soil science. Insights derived from this research, as well as the interdisciplinary approach that it develops, will apply to other groups of plants, particularly the large portion of plant diversity in which strong adaptations to soil conditions are observed. The proposed research will also advance understanding of North American plant diversity, foster international collaboration, result in the broad dissemination of research results within the scientific community, and benefit society through direct outreach in the form of guided hikes in Ceanothus habitats in the state of California, and writings directed at the general public.

Oaks (the flowering plant genus Quercus) include some of America's most ecologically and economically important trees. The approximately 255 oaks of the New World oak lineage dominate North American and Mexican woody plant biomass, biodiversity, ecology, and nutrient cycling. Despite the significant ecosystem services provided by oaks, the biodiversity of this genus is poorly understood. In this project, collaborators from The Morton Arboretum (IL), the University of Notre Dame (IN), Duke University (NC), University of Minnesota, and Universidad Nacional Autónoma de México will undertake a comprehensive systematic study of the oaks of the New World. The project will integrate next-generation genomic (DNA) sequencing, plant physiology, and direct study of plants in the field and museum collections to gain insights into the oak tree of life and the basic question of how oak traits, distributions, and diversity evolve in response to changes in habitat and climate.

Understanding of how oaks respond to shifts in climate and habitat is essential to conserving forest biodiversity and healthy forest ecosystems for future generations. The project will broadly disseminate findings and increase biodiversity awareness and understanding across diverse audiences in several ways: strengthening of an international oak collaboration among U.S., Mexican, and European researchers; training of undergraduate through postdoctoral biodiversity researchers; training K-12 teachers and their students in biodiversity science; and public outreach through museums, botanical gardens, and online venues.

The world’s approximately 425 oak species maintain species identity even while exchanging genes with their close relatives through hybridization. This history of evolution and genetic exchange has shaped the biodiversity of northern hemisphere ecosystems. Oaks are ecologically diverse, with related species often growing in close proximity but specializing on areas of the forest landscape that differ in soil texture and moisture level or in the frequency of natural fires. Gene exchange can move such ecological specializations between oak species, broadening their ranges and ability to respond to climate change. The impacts of these genetic exchanges may extend beyond the oaks themselves. Oaks host an estimated 1000 gall wasp species worldwide and highly diverse communities of fungi associated with their roots (as mycorrhizae) and inside their leaves (as endophytes). Using paired field surveys and common garden experiments the PIs will evaluate the effects of hybridization and introgression on the genetic, phylogenetic, and functional diversity of focal oak species and their symbionts in the US and China. This work will also provide inquiry-based K-12, undergraduate, and graduate education; critical natural history training to the public through a community-science initiative in oak phenology; and publications that will bring research to public audiences.

Two interdisciplinary teams of researchers, one based in the US and one in China, will investigate how genomic, functional, and phylogenetic diversity of oak trees shape the mycorrhizal fungi, endophytic fungi, and gall wasp and other insect communities that associate with them. Research will focus on two related groups of interbreeding species: bur oak (Quercus macrocarpa) and relatives in the US and bao li (Quercus serrata) and relatives in China. The project has three objectives, each conducted in parallel in China and the U.S. In Objective 1 the teams will perform range-wide phylogenomic surveys of natural populations to reconstruct genomic mosaics, characterize geographic patterns of leaf functional traits, and characterize functional and phylogenetic diversity of associated mycorrhizal fungi, leaf endophytic fungi, and gall wasps. In Objective 2 common gardens will be planted across climatic gradients to evaluate the effects of genetic variation and population differentiation on oak functional and spectral traits and relative fitness in different climates, and how these influence the phylogenetic and functional diversity of oak-associated fungal and insect communities. In Objective 3 the teams will use a second set of common garden experiments to evaluate how plant community and phylogenetic diversity affects focal oak species genetic, phylogenetic, and functional diversity. The project will provide an integrative perspective on how oak diversity within and among species impacts the broad diversity of oak-dominated ecosystems across the northern hemisphere.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.