Source: UNIVERSITY OF CALIFORNIA, DAVIS submitted to
ORIGIN AND EARLY EVOLUTION OF ANGIOSPERMS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
REVISED
Funding Source
Reporting Frequency
Annual
Accession No.
0167434
Grant No.
(N/A)
Project No.
CA-D-EVE-5918-H
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Oct 1, 2009
Project End Date
Sep 30, 2014
Grant Year
(N/A)
Project Director
Doyle, J.
Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671
Performing Department
Evolution and Ecology
Non Technical Summary
The main goal of this project is an improved picture of the first angiosperms (flowering plants), the dominant group of plants on earth and the basis of almost all human agriculture, and the early steps in their evolution. This is closely related to the origin of angiosperms, which is one of the great unsolved problems in evolutionary biology and paleontology. Although the evolutionary connections between angiosperms and other plant groups remain unclear, great progress in understanding the first angiosperms has been made in the past four decades, thanks to work in several areas: studies of the oldest fossil angiosperms, from the early part of the Cretaceous period (100-145 million years ago), which clarify general trends in early angiosperm evolution; computer methods for reconstructing evolutionary relationships among the members of a group based on their similarities and differences (cladistics); and the use of DNA sequences from living plants as a vast new source of data for these analyses. The work proposed here, which is a continuation of a Hatch project begun in 2004, involves pulling together published and new data on the structure of all parts of the plant (such as leaves, wood, flowers, pollen, fruits, and seeds) in the most ancient living lines of angiosperms; i.e., those that branched off near the base of the evolutionary tree. We plan to analyze our data on plant structure together with published molecular data (DNA sequences) from the same plants groups, using computer programs designed to find the evolutionary tree that agrees best with all the available information. Given such an evolutionary tree, the most likely course of evolution can be reconstructed by mapping presence or absence of structures, or different versions of structures, on the tree. To gain still better understanding of the evolution of living plant groups, early fossil flowers described by paleobotanists from Cretaceous rocks can be added to the analysis to determine their best position on the evolutionary tree, based on the features that are preserved. This procedure can reveal intermediate steps in the evolution of groups that are no longer represented in the living flora. Together, these approaches should lead to greatly improved understanding of the changes that occurred in the early evolution of angiosperms, how they led to the vast diversity of form and ecology in living plants, and how plants can be modified for human benefit.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
20624991060100%
Knowledge Area
206 - Basic Plant Biology;

Subject Of Investigation
2499 - Plant research, general;

Field Of Science
1060 - Biology (whole systems);
Goals / Objectives
(1) Revision, enlargement, and documentation of a morphological data set for phylogenetic (cladistic) analysis of evolutionary relationships among living 'basal' angiosperms, incorporating new data on morphological characters and improved evidence on ancestral states within groups derived from finer-scale analyses. Outputs will include a comprehensive data matrix for morphological characters of basal angiosperms and critical discussions of these characters, which will summarize current knowledge on the morphology of these groups and be useful to students of angiosperms as a whole. This should be an important resource for researchers studying the developmental and genetic basis of evolutionary changes in plant structure (evo-devo). (2) Phylogenetic analysis of these data combined with DNA sequences from the same plant groups, and analysis of the implications of the resulting trees for evolution of morphological characters. The goal of the combined phylogenetic analysis is a best 'total evidence' estimate of the basal angiosperm tree based on currently available information. Plotting of characters on this tree can in turn be used to reconstruct ancestral character states in angiosperms as a whole and in important subgroups and their various early modifications. (3) Integration of Early Cretaceous fossil taxa (mostly flowers described by other workers) into phylogenetic analyses of living basal angiosperms. This will involve interpreting, synthesizing, and scoring morphological characters of the fossils on the same terms as those of living taxa, including them in the morphological data set as additional taxa, and determining their most likely phylogenetic positions on the tree of living angiosperms. Results will be disseminated through talks at botanical and evolutionary meetings, journal articles and book chapters, and a book summarizing all the data and results, which should become an important reference for those interested in plant systematics, the evolution of morphological structures, and developmental-genetic mechanisms underlying evolutionary change. OBJECTIVES: (1) Revision, enlargement, and documentation of a morphological data set for phylogenetic (cladistic) analysis of evolutionary relationships among living 'basal' angiosperms, incorporating new data on morphological characters and improved reconstruction of ancestral conditions within groups based on finer-scale analyses. (2) Combination of these data with DNA sequences from the same groups and analysis of the implications of the resulting trees for evolution of morphological characters. (3) Integration of Cretaceous fossil taxa (mostly flowers described by other workers) into phylogenetic analyses of living basal angiosperms.
Project Methods
Most work in amassing the morphological data matrix has been accomplished, based on a survey of the botanical literature and studies of living, herbarium, and preserved specimens, but much effort is needed to organize the data for publication, including documentation of sources of evidence and the reasoning behind character definitions and interpretations of problematical structures. For the combined analysis of morphological and molecular data, we plan to collaborate with colleagues amassing molecular data on the same plant groups. Morphological and molecular data will be analyzed using standard computer programs for cladistic (parsimony) analysis, to obtain phylogenetic trees, and for reconstruction of character evolution on the trees obtained. Integration of Cretaceous fossils into the phylogeny of living plants will involve scoring of characters of fossil taxa based on descriptions in the paleobotanical literature and addition of these fossils to the morphological data matrix for living plants. The resulting morphological data set will be analyzed cladistically with fossils included one at a time or together, and with relationships of living groups fixed by constraint trees based on our best estimates of phylogenetic relationships, or combined with the molecular data set for living taxa, with fossils scored as unknown for molecular characters. This sort of global, explicit, and reproducible analysis should be an improvement over the traditional procedure of assigning fossils to living taxa based on more selective and subjective comparisons of their characters. Implications of the results for understanding the timing and course of evolution of living groups will be evaluated using the same programs for the study of character evolution on phylogenetic trees. Inferences for character evolution will be represented graphically with standard programs for plotting characters on phylogenetic trees, but results concerning the positions of fossils, a less well-developed topic, will be illustrated using more novel methods to indicate the best and next-best positions of fossils on the tree of living plants.

Progress 01/01/13 to 09/30/13

Outputs
Target Audience: Our contributions are of interest to researchers in a broad range of target areas in plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions, where primitive angiosperms are most diverse. They are also relevant to members of the general public interested in plant evolution, diversity, and conservation. Contributions in previous years on evolution of the family Annonaceae (cherimoya, soursop, etc.) should provide valuable perspective to researchers attempting to enhance the value of these tropical trees as fruit crops. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? In addition to the book and journal publications listed, results of this project were disseminated by the following four talks at scientific meetings and a seminar at a leading agricultural university in Vietnam: Brazilian Symposium on Paleobotany and Palynology, Rio de Janeiro, May 13-16, 2013: Recognizing angiosperm clades in the Early Cretaceous fossil record. Agora Paleobotanica, Ariño, Spain, July 9-13, 2013: Recognizing angiosperm clades in the Early Cretaceous fossil record. Botanical Society of America, July 27-31, 2013: Angiosperm clades in the Potomac Group: what have we learned since Hickey & Doyle 1977? American Association of Stratigraphic Palynologists, Oct. 20-24, 2013: Palynologicaal and molecular evidence on the origin of angiosperms: conflict, congruence, or both? Thai Nguyen University of Agriculture and Forestry, Vietnam, Nov. 8, 2013: What do we know about the origin of angiosperms? What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Doyle (2013) provides an overview of current understanding of the evolution of major morphological innovations in land plants, as clarified by phylogenetic analyses over the past three decades, as a chapter of a general treatise on the evolution of plant form. Sections on innovations in angiosperms are most closely related to the present project. This review was intended to be useful for instructors in introductory biology courses that cover the “tree of life,” as well as more advanced courses in paleobotany, plant morphology and anatomy, and plant systematics. It should also be a valuable reference for students, researchers, and faculty in the broad areas of plant structure, evolution, and diversity. Doyle & Endress (in press) essentially completes the part of this project devoted to placement of Early Cretaceous fossils in phylogenetic trees of living angiosperms, as revealed by molecular analyses. This study shows that several Early Cretaceous fossils belong within the clade (crown group) that includes all living members of Nymphaeales (water lilies), which molecular analyses indicate are one of the three most ancient angiosperm lines. These results imply that Nymphaeales had become aquatic by this time, contrary to molecular dating analyses that implied that the crown group did not originate until much later. It also confirms that several of the most common early angiosperm fossils are related to the now-minor family Chloranthaceae, notable for its extremely simplified flowers. These results confirm that the simple flowers of Chloranthaceae are the result of an early trend for floral reduction, by showing intermediate stages in simplification of the flowers. They also show that two fossils that have been thought to be related to monocots and Piperales are more likely related to Chloranthaceae, or to the possibly related aquatic plant Ceratophyllum, whose origin and phylogenetic position have been enigmatic. Massoni et al. (in press) makes use of previous analyses in this project and those of other workers treating fossils that phylogenetic analyses indicate belong in Magnoliidae, the largest clade of primitive angiosperms and a major focus of this project (familiar members are magnolia, cherimoya, laurels, avocado, and black pepper. Its specific purpose is to document the geologic age and phylogenetic position of these fossils so they can be used in defining calibration points (minimum ages of common ancestors in millions of years) in molecular dating analyses, which are a major focus of current research in this field.

Publications

  • Type: Other Status: Published Year Published: 2013 Citation: Doyle, J. A., 2013. Phylogenetic analyses and morphological innovations in land plants. In: The evolution of plant form, Ambrose, B. A., Purugganan, M. D., eds. (Annual Plant Reviews vol. 45), 1-50. Wiley-Blackwell, Oxford.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Integrating Early Cretaceous Fossils into the Phylogeny of Living Angiosperms: ANITA Lines and Relatives of Chloranthaceae James A. Doyle and Peter K. Endress International Journal of Plant Sciences, Vol. 175, No. 5 (June 2014), pp. 555-600 (Submitted 2013)
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Massoni, J., Doyle, J. A., Sauquet, H., in press. Fossil calibration of Magnoliidae, and ancient lineage of angiosperms. Palaeontologia Electronica. (Submitted 2013)


Progress 01/01/12 to 12/31/12

Outputs
OUTPUTS: This project focuses on evolution of the most ancient lines of living angiosperms (flowering plants) and the oldest fossil angiosperms of the Cretaceous period, as inferred from phylogenetic analyses of morphological and molecular data. Doyle & Le Thomas (2012) and Pirie & Doyle (2012) are the culmination of the part of this project devoted to the tropical family Annonaceae, the largest family of "primitive" angiosperms. This family includes the trees that produce cherimoya, soursop, and related fruits, which are the focus of increasing agricultural research in Brazil and other countries. Doyle & Le Thomas (2012) compiled and evaluated all existing data on pollen morphology of Annonaceae and synthesized these data by plotting the evolution of pollen characters on the most recent molecular phylogenetic trees. Pirie & Doyle (2012) presented a general review of the thorny problems of dating the evolution of modern plants based on the fossil record and analysis of molecular divergence between species, which should be of value for students of other groups than Annonaceae, and a critical review of relevant fossils and molecular analyses of the ages of Annonaceae and groups within them. Both papers are in a special journal issue on Annonaceae that should become a standard reference for researchers working on all aspects the family. Doyle (2012) is a general review of the current status of the origin of angiosperms, emphasizing the relations between data from the fossil record and from molecular phylogenetic analyses. At the International Organisation of Paleobotany Conference and International Palynological Congress in Tokyo (August 2012), I presented results of continuing analyses by Peter Endress and myself of the position of early angiosperm fossils in molecular phylogenies of living angiosperms, specifically fossils related to the most ancient branches of the evolutionary tree of angiosperms (Amborella, water lilies, Austrobaileyales) and to the now-obscure family Chloranthaceae, which was one of the most widespread groups during the early expansion of angiosperms. PARTICIPANTS: Peter Endress is a retired professor at the Institute of Systematic Botany at the University of Zurich in Switzerland, who is a world expert on morphology and evolution of angiosperm flowers. Annick Le Thomas is a retired researcher and professor at the Museum National d'Histoire Naturelle in Paris and an expert on the systematics and pollen morphology of Annonaceae. Michael Pirie is a postdoctoral researcher at the University of Stellenbosch, South Africa, and an expert on molecular systematics, evolution, and biogeography of Annonaceae. TARGET AUDIENCES: Our contributions are of interest to researchers in a broad range of target areas in plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions, where primitive angiosperms are most diverse. They are also relevant to members of the general public interested in plant evolution, diversity, and conservation. The studies on Annonaceae should provide valuable perspective to researchers attempting to enhance the value of these tropical trees as fruit crops. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Doyle & Le Thomas (2012) confirmed the conclusion of earlier analyses that monosulcate pollen with granular exine structure was ancestral in Annonaceae but suggested that columellar exine structure evolved earlier within the family that previously assumed, and that reversals in exine structure were more common. We highlighted recent findings that the thin germination area in some species that shed their pollen as tetrads comes to lie at the center of the tetrad by rotation of the microspores but not in others, and that future observations of pollen development in species not yet studied may affect ideas on the evolution of apertures across the family. Pirie & Doyle (2012) reviewed recent fossil discoveries that push back the origin of Annonaceae to early in the Late Cretaceous, bringing fossil data more in line with molecular dating results, but also showed that that different molecular dating methods give substantially different ages for the two main subgroups of the family, apparently as a result of different rates of molecular evolution and different approaches of the methods for dealing with them. We recommend caution in the use of methods that make assumptions on how far groups are likely to extend back before their first fossil appearance and argue that molecular dates be generally viewed as minimum ages. Doyle (2012) showed that the consistency between fossil sequences and molecular phylogenies on trends in the main radiation of angiosperms supports the concept that the radiation was occurring in the Early Cretaceous, and that this agreement contradicts molecular dating studies that imply that angiosperms originated and began diversifying long before the Cretaceous. The hypothesis that early angiosperms were ecologically restricted to wet understory environments would allow a long pre-Cretaceous history of very primitive angiosperms, but not angiosperms as diverse as is implied by some dating analyses.

Publications

  • Doyle, J. A., 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301-326.
  • Doyle, J. A., Le Thomas, A., 2012. Evolution and phylogenetic significance of pollen in Annonaceae. Botanical Journal of the Linnean Society 169: 190-221.
  • Pirie, M. D., Doyle, J. A. 2012. Dating clades with fossils and molecules: the case of Annonaceae. Botanical Journal of the Linnean Society 169: 84-116.


Progress 01/01/11 to 12/31/11

Outputs
OUTPUTS: This project focuses on evolution of the most ancient lines of living angiosperms (flowering plants) and the oldest fossil angiosperms of the Cretaceous period, as inferred from phylogenetic analyses of morphological and molecular data. Doyle & Endress (2011) synthesized results of our work on early evolution of the flower, in which we mapped floral characters from the extensive data set on morphology of living angiosperms that we have amassed over the past 13 years on the most recent phylogenetic trees based on molecular data. This approach allowed us to reconstruct the architecture of the flower in the most recent common ancestor of angiosperms and at various key stages in their early evolution. I presented many of these results, along with those obtained in earlier analyses on the relationships of angiosperms with other living and fossil seed plants (gymnosperms), at a symposium on floral evolution at the International Botanical Congress in Melbourne, Australia in July 2011 and in a seminar at the University of Munich in November 2011. At the Melbourne congress I took part in a meeting of the "eFlower" project, organized by Herve Sauquet at the University of Paris, which intends to make our data and that of other members of the project available to researchers in plant evolution and related fields in an online data base. In a research trip to Zurich in November 2011, Endress and I continued our analyses of the position of early angiosperm fossils; analyses of fossils related to monocots, magnoliids (such as magnolias and laurels), and eudicots (such as lotus, sycamore, and box) were published in earlier review periods. These analyses involve fossil flowers and associated leaves described largely by other workers that appear to be related to the most ancient branches of the evolutionary tree of angiosperms, including the New Caledonian shrub Amborella, Nymphaeales (water lilies), Illicium (star anise), and the now obscure family Chloranthaceae, notable for its highly simplified flowers, which was one of the most widespread groups during the early expansion of angiosperms. PARTICIPANTS: Peter K. Endress is a recently retired but active professor at the Institute of Systematic Botany at the University of Zurich in Switzerland, who is a world expert on morphology and evolution of flowers in angiosperms. TARGET AUDIENCES: Our contributions are of interest to researchers in a broad range of target areas in plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions, where primitive angiosperms are most diverse. They are also relevant to members of the general public interested in plant evolution, diversity, and conservation. Hopefully the results of our analyses of floral evolution will provide a valuable evolutionary framework for molecular-genetic studies on the evolution of development (evo-devo) and the use of an evo-devo perspective for modification of flower and fruit morphology in crop species by genetic engineering. Our use of floral diagrams is especially useful for communicating conclusions on the evolution of floral types in a graphic, intuitive fashion. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Doyle & Endress (2011), which built on a more technical analysis published in 2009, was intended to communicate more graphically our inferences on the architecture of flowers at key stages in the early evolution of angiosperms, and evolutionary changes involved in going from one type to the next, using floral diagrams. We were able to reconstruct the flower of the recent common ancestor of angiosperms as having many undifferentiated sterile parts (tepals), many stamens, and a moderate number of carpels containing one ovule (seed) each, although we could not determine whether parts were arranged in a spiral or in regular whorls of three. We inferred that the huge clade called mesangiosperms, which includes 99.9% of living angiosperm species, originally had a floral diagram that is not directly retained in any living descendants, with parts in whorls of three: three or more whorls of tepals, two whorls of stamens, and several carpels. The number of whorls of tepals was reduced to two in monocots, resulting in the distinctive floral architecture of lilies, onions, and palms. In magnoliids, the flowers of magnolias, spicebush, and relatives, which have larger numbers of spiral parts, have traditionally been considered primitive, but our results indicate that they more likely represent a partial reversal to the ancestral type. The typical flowers of eudicots, with well-differentiated sepals and petals and parts in fives (less commonly fours), appear to be derived from simpler flowers in early eudicots, which had no petals, only sepal-like tepals, and parts in cycles of two. These results should provide a valuable perspective on the evolution and development of the familiar flowers of eudicots and monocots, which include most crop species.

Publications

  • Doyle, J. A., Endress, P. K., 2011. Tracing the early evolutionary diversification of the angiosperm flower. Flowers on the tree of life (Wanntorp, L., Ronse De Craene, L. P., eds.), 88-119. Cambridge University Press.


Progress 01/01/10 to 12/31/10

Outputs
OUTPUTS: This project focuses on evolution of living primitive angiosperms (flowering plants) and the oldest Cretaceous fossil angiosperms, based on phylogenetic analyses of morphological and molecular data. Doyle & Endress (2010) summarized a large portion of the project to date by presenting analyses of the phylogenetic position of described Early Cretaceous fossils that appear to belong to the magnoliid and eudicot clades, complementing earlier papers on fossil monocots and the controversial aquatic angiosperm Archaefructus. This leaves fossils believed to belong to the basal "ANITA" grade of angiosperms and the Chloranthaceae, an early line that underwent a remarkable degree of floral simplification. This paper includes the latest version of the whole morphological phylogenetic data matrix that we have been compiling and refining since 1998; the portion dealing with floral characters was published in 2009. This paper appeared in the Journal of Systematics and Evolution, a Chinese journal that is aspiring to major international status. Many of the results were included in talks at the 8th European Palaeobotany-Palynology Conference in Budapest, Hungary (Early Cretaceous monocots); the meeting of the American Association of Stratigraphic Palynologists in Halifax, Canada (relations of fossil and molecular evidence on the early evolution of angiosperm pollen); the 10th Latin American Botanical Congress in La Serena, Chile (keynote lecture on the origin of angiosperms); and the UC Berkeley Integrative Biology seminar series (origin of angiosperms). Doyle (2010) was a commentary on a paper on pollen morphology in conifers (specifically the functional significance of air sacs or "wings"), but it made original contributions in exploring the evolutionary significance of sacs in a phylogenetic framework and the implications of sacs for controversies on the morphology and biology of fossil seed plants. This paper appeared in the New Phytologist, a widely circulated international botanical journal. Aspects of this project dealing with fossil and molecular evidence on dating of groups within the important tropical magnoliid family Annonaceae were presented at the Botanical Society of America meeting in Providence, RI. PARTICIPANTS: Peter K. Endress is a recently retired professor at the Institute of Systematic Botany at the University of Zurich in Switzerland, who is a world expert on morphology and evolution of flowers in angiosperms. TARGET AUDIENCES: These contributions are of interest to researchers in a broad range of target areas in plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions. They are also relevant to members of the general public interested in plant evolution, diversity, and conservation. Doyle & Endress (2010) is of broad interest for those concerned with the relation between fossil and molecular evidence on the early evolution of angiosperms, by providing the first formal analyses of the position of many of the most important Early Cretaceous fossils in the phylogeny of living angiosperms. This is in turn important for the many current studies that use the amount of molecular divergence between species as evidence on the age of angiosperm groups, since they provide more solid calibration points for ages of branches in molecular trees. The data set in this paper should be a major resource and a framework for future analyses by botanists interested not only in the position of other early angiosperm fossils, but also in the evolution of morphological characters and their adaptive significance, developmental-genetic basis ("evo-devo"), and potential modification in genetic engineering. Doyle (2010) is of interest for those involved in the pollination biology of conifers, an important component of forestry research, as well as in pollination biology of fossil plants. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The analyses of Doyle & Endress (2010) confirmed previously proposed relationships of Cretaceous fossil flowers and pollen with the living families Magnoliaceae (Magnolia, etc.), Winteraceae, Nelumbonaceae (lotus), Platanaceae (sycamores), and Buxaceae (boxwoods), but they implied that the fossils were more primitive sister groups of the modern families rather than members nested within them. However, the fossil flower Virginianthus may be sister to either the lauralean family Calycanthaceae (including spicebush), as originally proposed, or the remaining Laurales, while Mauldinia, assigned by its original describers to Lauraceae (a major tropical and subtropical family that includes avocado and cinnamon), appears to be sister to both Lauraceae and its sister family Hernandiaceae, implying that Hernandiaceae were derived from an ancestor with essentially lauraceous flowers. Endressinia appears to represent an extinct line within Magnoliales. These results provide important constraints on the ages of key nodes near the base of the angiosperm phylogenetic tree for future molecular dating analyses. The data set included in this paper extends that published in Endress & Doyle (2009), which emphasized floral characters, by adding all the non-floral characters that we have compiled over the past 13 years. Besides reviewing experiments that confirmed the value of air sacs in flotation of pollen in the micropylar canal of pinaceous conifers, Doyle (2010) used results of phylogenetic analyses of living and fossil seed plants to show that air sacs evolved earlier and are homologous across more groups than might be inferred from studies of living plants alone, and showed that the flotation hypothesis favors interpretation of the seed-bearing structures of glossopterids, a Permian seed plant group often implicated in the origin of angiosperms, as having the seed-bearing surface oriented downward.

Publications

  • Doyle, J. A., Endress, P. K., 2010. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. Journal of Systematics and Evolution 48: 1-35.
  • Doyle, J. A., 2010. Function and evolution of saccate pollen. New Phytologist 188: 6-9.


Progress 01/01/09 to 12/31/09

Outputs
OUTPUTS: This project focuses on evolution of living primitive angiosperms (flowering plants) and the oldest Cretaceous fossil angiosperms, based on phylogenetic analyses of morphological and molecular data. One contribution (Doyle 2009) presented an updated synthesis of the significance of so-called granular structure of the pollen wall (exine) in the light of phylogenetic analyses. Most angiosperms have columellar exine structure, with an inner and outer layer connected by minute columns, while many gymnosperms have alveolar structure, with the middle layer consisting of chambers (alveolae) surrounded by partitions. The granular type, with round granules between the inner and outer layers, was first recognized in the 1970s both in some angiosperms and in some gymnosperms, which led several authors (myself included) to suggest it was ancestral in angiosperms. This paper reassessed these ideas in a phylogenetic framework, based largely on analyses of DNA sequence data. These observations were disseminated through the Review of Palaeobotany and Palynology, the leading journal in this field, and distribution of reprints and pdfs. Endress & Doyle (2009) provided a detailed synthesis of the implications of phylogenetic analyses for the original morphology of the angiosperm flower and its component parts. This paper was a culmination of 12 years of collaboration with Endress on a morphological phylogenetic data matrix for basal angiosperms, presented in its most comprehensively documented form in this paper, which we used to reconstruct the most likely course of evolution of floral characters on a range of current phylogenetic trees based primarily on molecular data. We also used this data set to evaluate the phylogenetic position of the controversial fossil Archaefructus, one of the oldest known angiosperms, from the Early Cretaceous of China. This paper appeared in a Darwin centenary issue of the American Journal of Botany devoted to what Darwin called the "abominable mystery" of the origin and rise of angiosperms, and according to the AJB web site, it was the 25th most read paper ever published in AJB during January 2010 and second most read article from the Darwin issue. This issue stimulated articles on the origin of flowers in Science (Elizabeth Pennisi, April 3, 2009) and the New York Times (Carl Zimmer, Sept. 8, 2009); I was interviewed and cited extensively in the latter. I also summarized the results in an invited talk at the European Systematics Congress in Leiden in August 2009, and I presented the aspects concerning Archaefructus in an invited talk at a meeting on systematics and evolution in Shenzhen, China and a seminar in Kunming, China. PARTICIPANTS: Peter K. Endress is a recently retired professor at the Institute of Systematic Botany at the University of Zurich in Switzerland, who is a world expert on morphology and evolution of flowers in angiosperms. TARGET AUDIENCES: These contributions are of interest to researchers in a broad range of target areas in plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions. They are also relevant to members of the general public interested in evolution, plant diversity, and conservation. Endress & Doyle (2009) is of especially broad interest as the latest synthesis of the implications of recent molecular phylogenetic results for the nature of the ancestral flower and its early modifications, which as noted above prompted several articles in the general scientific and popular press, including Science and the New York Times. The data set presented in this article should be a major resource and a basis for future analyses by future workers interested in the evolution of floral characters and their ecological and adaptive significance (e.g., in pollination biology and seed dispersal), developmental-genetic basis ("evo-devo"), and potential modification in genetic engineering. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Doyle (2009) showed that the current picture of relationships within angiosperms contradicts the older view that granular exine structure was ancestral in angiosperms, since the lines that branch off successively at the base of molecular phylogenetic trees all have columellar structure, and granular structure is restricted to several clades located further up in the tree, notably several families of the magnoliid orders Magnoliales and Laurales (including Annonaceae, which contain the fruit crop cherimoya, and Lauraceae, which include avocado and cinnamon), and several groups within the eudicots (a clade made up of ca. 75% of all angiosperm species), including a major subgroup of the wind-pollinated order Fagales (e.g., birches and walnuts). Similarly, in gymnosperms, phylogenetic results imply that alveolar structure was ancestral and granular structure evolved in a large subgroup of conifers and in Gnetales, independently from granular structure in angiosperms. However, it is still systematically important as a morphological character that unites each of these groups. Endress & Doyle (2009) showed that current phylogenetic results confirm earlier but by no means universally accepted views that the common ancestor of living angiosperms had flowers with an undifferentiated perianth (tepals), fairly numerous stamens, and more than one carpel. However, it is ambiguous whether the parts were arranged in a spiral or in whorls of three, and whether the flower was bisexual or unisexual. Less expected inferences are that the ancestral carpel type grew up like a tube (ascidiate) rather than a leaf folded down the middle (plicate), as shown in many textbooks, and probably had a single apical ovule. Although molecular analyses show that there are several groups with extremely simple flowers near the base of the angiosperm tree (Hydatellaceae, Chloranthaceae, Ceratophyllum), which some recent authors have suggested are primitive, it is most parsimonious to assume that these were derived from flowers with many parts, in some cases as an adaptation to aquatic habitats. This also applies to the fossil Archaefructus, which has been interpreted as more basal and more primitive than all living angiosperms, but which our analyses suggest is related to either Hydatellaceae, in the Nymphaeales (water lilies), or Ceratophyllum (also a water plant). We inferred that the common ancestor of the vast majority (99.9%) of living angiosperms had flowers with several whorls of three perianth parts and two whorls of stamens, which was simplified in monocots and the first eudicots but underwent an increase in numbers of parts and a shift to spiral arrangment within magnoliids (Magnoliales and Laurales), resulting in flowers that look more "primitive" than they actually are.

Publications

  • Doyle, J.A. 2009. Evolutionary significance of granular exine structure in the light of phylogenetic analyses. Review of Palaeobotany and Palynology 153: 198-210.
  • Endress, P.K., Doyle, J.A. 2009. Reconstructing the ancestral angiosperm flower and its initial specializations. American Journal of Botany 96: 22-66.


Progress 01/01/08 to 12/31/08

Outputs
OUTPUTS: This project focuses on evolution of living primitive angiosperms (flowering plants) and the oldest Cretaceous fossil angiosperms, based on phylogenetic analyses of morphological and molecular data. One contribution (Doyle 2008), which falls partly outside the main focus of the project but is closely related to it, is an analysis of the origin of the angiosperm flower and its parts in the context of the phylogeny of seed plants as a whole. Seed plant phylogeny is an area of controversy and conflict between studies based on morphological and molecular data. This analysis addressed these conflicts and tried to synthesize the two sorts of data. More directly related to the Experiment Station project, it also analyzed the position of the Early Cretaceous fossil Archaefructus, from China, which has been interpreted as a more primitive relative of living angiosperms. This information has been disseminated in the International Journal of Plant Sciences, and the aspects related to Archaefructus were presented in a talk at the congress of the International Organization of Palaeobotany in Bonn, Germany and seminars in Wellington, New Zealand and Zurich, Switzerland. Much of my research in 2008 was part of a continued collaboration with Peter Endress on an expanded and improved data set of morphological characters in primitive angiosperms. This led to a paper on reconstruction of the ancestral angiosperm flower and its early evolution, based on molecular phylogenies of basal angiosperms, which was submitted and accepted in 2008 but not published until 2009. However, we used this data set and that of Doyle (2008) in Doyle, Endress and Upchurch (2008) to address the question of whether or not monocots occur in the Early Cretaceous fossil record, which has become contentious in recent years. This paper used cladistic analyses of these data to evaluate whether Early Cretaceous fossils described as monocots by myself and other workers are indeed related to this group. The journal in which the results are published is not widely circulated in the US, but this will be mitigated by distribution of reprints and pdfs, and I plan to present the results at the 2009 meeting of the Botanical Society of America. Doyle, Manchester and Sauquet (2008) is an outgrowth of previous research on the basal angiosperm order Magnoliales, which has been a major focus of this project. In it, we describe the oldest known fossil seed that can be related to Myristicaceae, the nutmeg family, from the Eocene (ca. 50 MY ago) of England. Myristicaceae have a pantropical geographic distribution that suggests a Cretaceous origin, but definite myristicaceous fossils older than the Miocene (ca. 15 MY ago) have been lacking, and molecular data suggest that the living clade (crown group) is surprisingly young. These results were presented at the meeting of the Botanical Society of America in 2007 and published in the journal Systematic Botany. PARTICIPANTS: Peter Endress is a recently retired professor at the Institute of Systematic Botany at the University of Zurich in Switzerland, who is a world expert on morphology and evolution of flowers in angiosperms. Steven Manchester is Curator of Paleobotany at the Florida Museum of Natural History at the University of Florida and a leading expert on fossil fruits and seeds and their implications for the geologic history and biogeography of angiosperms. Herve Sauquet is a lecturer at the University of Paris who was involved earlier in my research program as a visiting graduate student in 2001 and 2003, as part of his thesis research on phylogeny and evolution of the Myristicaceae and related families of magnoliid angiosperms. Garland Upchurch (my first PhD student) is professor in the Department of Biology at Texas State University, who works on leaf architecture and epidermal (cuticle) anatomy of living and fossil angiosperms and their application to fossil floras and paleoclimates. TARGET AUDIENCES: These contributions are of interest to researchers in a broad range of areas of plant biology: systematics, morphology, paleobotany, development, biogeography, and ecology, especially of tropical regions. They are also relevant to members of the general public interested in evolution, plant diversity, and conservation. The distinctive parallel-veined leaf architecture of monocots, clarified in Doyle, Endress and Upchurch (2008), is of prime importance for physiological ecology and agriculture but has been relatively neglected by botanists. Myristicaceae are important members of tropical forests, and a better understanding of their geologic history, as provided in Doyle, Manchester and Sauquet (2008), may provide perspective for those involved in conservation and sustainable use of these communities. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The paper on origin of the flower (Doyle 2008) helps to resolve the conflict between morphological and molecular data by showing that the hypothesis that the living gymnosperm group Gnetales is related to angiosperms (based on morphological data) and the hypothesis that Gnetales are instead related to conifers (as found in increasing numbers of molecular analyses) are equally consistent with a new morphological data set. When this data set is analyzed with living groups fixed in a molecular arrangement, angiosperms are most closely related to several fossil groups - glossopterids, Pentoxylon, Bennettitales, and Caytonia - that have been widely discussed as angiosperm relatives. These results are consistent with proposed homologies between the angiosperm carpel and the cupule-bearing structures of glossopterids and Caytonia, with the outer integument of the angiosperm ovule derived from the ovule-enclosing cupule of the fossils. Instead of being more basal than all living angiosperms, the fossil Archaefructus is more likely an early lineage within angiosperms that underwent floral reduction as an adaptation to an aquatic habitat, specifically related to Hydatellaceae, aquatic plants formerly considered to be monocots but shown in 2007 to belong to Nymphaeales (water lilies). The article on Cretaceous monocots (Doyle, Endress and Upchurch 2008) clarifies the often confused distinctions among pollen and leaf characters of monocots, other angiosperms, and gymnosperms. Our analyses show that some Early Cretaceous fossils that were originally interpreted as monocots but have been more recently questioned (fossil pollen grains called Liliacidites and leaves called Acaciaephyllum) are indeed most parsimoniously assigned to the monocots. However, two other fossil pollen types that have been compared with monocots, Pennipollis and Similipollis, which have been associated with fossil flowers in Portugal, appear to be related to other groups of basal angiosperms, respectively Chloranthaceae and Austrobaileyales. The fossil seed described in Doyle, Manchester and Sauquet (2008) is older than molecular dates for the family Myristicaceae, but we show that this may not be a conflict, since analyses of the phylogenetic position of the fossil, based on a data set developed earlier in this project, show that it can be equally parsimoniously placed in the crown group of Myristicaceae or on the stem lineage leading to it. The discussion of problems involved in distinguishing crown vs. stem relationships should be useful in evaluating other recent cases of apparent conflicts between the ages of groups based on fossil and molecular data.

Publications

  • Doyle, J.A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169: 816-843.
  • Doyle, J.A., Manchester, S.R., Sauquet, H. 2008. A seed related to Myristicaceae in the Early Eocene of southern England. Systematic Botany 33: 636-646.
  • Doyle, J.A., Endress, P.K., Upchurch, G.R. 2008. Early Cretaceous monocots: a phylogenetic evaluation. Acta Musei Nationalis Pragae, Series B, Historia Naturalis 64(2-4): 59-87.


Progress 01/01/07 to 12/31/07

Outputs
This project focuses on evolution of living primitive angiosperms (flowering plants) and the oldest Cretaceous fossil angiosperms, based on phylogenetic analyses of morphological and molecular data. I have continued to collaborate with Peter Endress (Zurich) on an expanded and improved data set of morphological characters in primitive angiosperms. In Endress & Doyle (2007), we clarified the distinction between spiral and whorled arrangement (phyllotaxis) of floral parts and used our data set to reconstruct the early evolution of this character in angiosperms. Traditionally, many authors assumed that whorled phyllotaxis was derived from spiral, but our analysis showed that switches in both directions were common in early angiosperm evolution and not completely correlated between the sterile perianth (tepals, sepals, and petals) and the reproductive parts (stamens and carpels). Saarela et al. (2007), based on collaboration with Sean Graham (Vancouver) and coworkers, presented molecular evidence that Hydatellaceae, a family of minute aquatic plants that were formerly assumed to be monocots, are instead related to Nymphaeales (water lilies), one of the oldest angiosperm lines. When we added Hydatellaceae to the Doyle & Endress morphological data set, we obtained exactly the same result, reaffirming the value of morphology in unraveling difficult relationships. Cantino et al. (2007) proposed names for major groups of vascular plants, from clubmosses and ferns through angiosperms, using the PhyloCode system of nomenclature, which defines groups based directly on their presumed phylogenetic relationships. These include both recently recognized groups and traditional groups confirmed by molecular phylogenetic analyses, many of which had only informal names, such as "core eudicots." Some authors have argued that systems based on the PhyloCode should replace current "Linnaean" systems based on the International Code of Botanical Nomenclature, but the PhyloCode can also be used in parallel with the ICBN to name groups at intermediate levels in the hierarchy that are not conveniently treated by the ICBN. Doyle (2007) synthesized data on leaf architecture (leaf form and venation) across the angiosperms, a topic last treated at this scale in 1975, in the framework of molecular and morphological phylogenetic analyses. This showed that leaf characters are more congruent with current molecular phylogenies than with systems that existed in 1975 and suggested novel hypotheses on the evolution of leaf characters, for instance that the widespread rosoid tooth type, seen in economically important groups such as Vitaceae (grapes) and Rosaceae (including many berry and fruit tree crops), was derived from the chloranthoid tooth of basal angiosperms, and that the huge asterid clade was united by a shift from palmate to pinnate venation. Annick Le Thomas (Paris) and I submitted an updated synthesis of pollen evolution in Annonaceae based on phylogenetic trees obtained in the latest molecular analyses, for a book on this large tropical family.

Impacts
Angiosperms are the dominant plants in modern terrestrial ecosystems and the basis of almost all human agriculture. Improved understanding of their origin and diversification may have practical impacts through the new insights it provides on plant genetics, pollination biology, and development of flowers and fruits. Our publications serve as basic references on morphological characters of leaves, flowers, fruits, seeds, and pollen in angiosperms and allow more reliable reconstruction of changes during early angiosperm evolution. Understanding of past evolutionary changes may provide perspective on the practicality of modifying corresponding traits in crop plants, and it is essential for the rapidly expanding field of evolutionary genetics of plant development ("evo-devo"), which in the long term is certain to have practical value in genetic engineering. Thus the Endress & Doyle (2007) paper is of broader interest in clarifying distinctions in floral phyllotaxis, about which there is much confusion, in both wild and cultivated plants. The Doyle (2007) paper on leaf architecture will hopefully focus more attention on evolutionary changes in leaf morphology, an area that has been neglected and poorly understood but has great practical importance for crop ecology and yields, by calling attention to previously unrecognized or poorly understood leaf features and modifications. An evolutionary prespective may also help in development of traditional and new crops in tropical families such as Annonaceae, in which cherimoya is already a significant fruit crop and other genera (such as Asimina - pawpaw) are under investigation for agricultural purposes. Many living primitive angiosperms are important members of restricted and threatened plant communities in the tropics and subtropics, and efforts to conserve them may also contribute to preservation and sustainable use of their endangered habitats and plant and animal associates. The Cantino et al. (2007) paper is a major step toward a phylogenetic classification of plants, a desirable goal from both theoretical and practical perspectives, since understanding of relationships is essential in the search for plants with useful characteristics. The PhyloCode project has a strong outreach component, since it intends to make its classifications available on line both to scientists in other areas of plant biology and to the general public. This should make it much easier for members of the broader community to grasp and apply the ongoing advances in understanding of relationships among plant groups.

Publications

  • Cantino, P.D., J.A. Doyle, S.W. Graham, W.S. Judd, R.G. Olmstead, D.E. Soltis, P.S. Soltis and M.J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56:822-846.
  • Doyle, J.A. 2007. Systematic value and evolution of leaf architecture across the angiosperms in light of molecular phylogenetic analyses. Courier Forschungs-Institut Senckenberg 258:21-37.
  • Endress, P.K. and J.A. Doyle. 2007. Floral phyllotaxis in basal angiosperms: development and evolution. Current Opinion in Plant Biology 10:52-57.
  • Saarela, J.M., H.S. Rai, J.A. Doyle, P.K. Endress, S. Mathews, A.D. Marchant, B.G. Briggs and S.W. Graham. 2007. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446:312-315.


Progress 01/01/06 to 12/31/06

Outputs
This project focuses on evolution of living primitive angiosperms (flowering plants) and the oldest Cretaceous fossil angiosperms, based on phylogenetic analyses of morphological and molecular data. I have continued to collaborate with Peter Endress (Zurich) on an expanded and improved morphological data set for primitive angiosperms. In two in-press articles, we used this data set to analyze early evolution of the arrangement of floral parts and (with molecular systematist Sean Graham and coworkers, Vancouver) to show that Hydatellaceae, a family of minute aquatics formerly assumed to be monocots, are actually related to Nymphaeales (water lilies). At a conference in Prague in September 2006 we used these data to evaluate the most likely placement of Cretaceous fossils in the phylogenetic tree of living angiosperms. In Scharaschkin and Doyle (2006), Tanya Scharaschkin (Queensland University of Technology) and I presented further results on Anaxagorea, the most basal evolutionary line in the large tropical family Annonaceae. This paper used our phylogenetic analyses of the genus, published in 2005, to reconstruct the evolution of morphological characters. Several features of Anaxagorea that are unusual in Annonaceae have been interpreted as primitive, such as an adaxial plate of xylem in the leaf midrib, leaflike stamens, and inner staminodes, all conditions found in other Magnoliales. However, the status of these features was uncertain because they are not present in all species of Anaxagorea. Inferred relationships within Anaxagorea imply that absences of these features are due to loss and their presence is primitive. They also indicate that conical floral buds, reduced inner petals, cuticle striations, and stigma shape are useful in defining natural groups within Anaxagorea. Doyle (2006) updated the phylogeny of living and fossil seed plants and the origin of angiosperms. Earlier morphological analyses placed angiosperms in an "anthophyte" clade that also included fossil Bennettitales and the living gymnosperm order Gnetales, but molecular data place Gnetales in conifers. Critical examination indicated that several morphological characters thought to support the anthophyte hypothesis are significantly different in Gnetales and angiosperms, while more recently recognized similarities favor a relationship of Gnetales and conifers. Analysis of a data set incorporating these observations still favored the anthophyte hypothesis, but a conifer-Gnetales connection was almost as strongly supported. Analysis of this data set with living groups constrained into the arrangement inferred from molecular data indicated that fossils formerly associated with angiosperms may still be related, namely Bennettitales, Pentoxylon, Glossopteridales, and Caytonia. This supports proposed homologies between the angiosperm bitegmic ovule and the cupules of glossopterids and Caytonia, with the number of ovules per cupule reduced to one and the cupule wall converted into the outer integument, and between the angiosperm carpel and seed-bearing stuctures of glossopterids, with one or more cupules attached to the adaxial side of a leaf.

Impacts
Angiosperms are the dominant plants in modern terrestrial ecosystems and the basis of almost all human agriculture. Improved understanding of their origin and diversification may have practical impacts through the new insights it provides on plant genetics, pollination biology, and development of flowers and fruits. Our publications serve as basic references on morphological characters of flowers, fruits, seeds, and pollen in angiosperms and allow more reliable reconstruction of morphological changes during early angiosperm evolution. Such information is essential for the current renewed interest in plant development in an evolutionary framework ('evo-devo'), and if it is combined with a better understanding of the genetic basis for the inferred evolutionary changes it may have practical value in genetic engineering of crops. An evolutionary prespective may also be valuable in improvement of traditional and new crop species in tropical families such as Annonaceae, in which cherimoya is already a significant fruit crop and other genera (such as Asimina - pawpaw) are under investigation for agricultural purposes. Many living primitive angiosperms are important members of restricted and threatened plant communities in the tropics and subtropics, and efforts to conserve them may also be of value in preservation and sustainable use of their endangered habitats and plant and animal associates.

Publications

  • Scharaschkin, T. and J.A. Doyle. 2006. Character evolution in Anaxagorea (Annonaceae). American Journal of Botany 93:36-54.
  • Doyle, J.A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133:169-209.


Progress 01/01/05 to 12/31/05

Outputs
This project focuses on reconstruction of evolutionary relationships among living primitive angiosperms (flowering plants) and the oldest fossil angiosperms from Cretaceous sediments, based on phylogenetic analyses of morphological and molecular data. I have continued to collaborate with Peter Endress (Zurich) on an enlarged and refined version of a morphological data set for primitive angiosperms that we published in 2000, based on characters from all parts of the plant. Our hope is that this data set will be a basic resource in the ongoing revival of interest in plant morphology and development in an evolutionary framework (evo-devo), as well as in integrating fossils into the phylogeny of living angiosperms, now largely based on molecular sequence data. Toward this goal I completely revised and updated pollen characters and published the results in a paper on early pollen evolution in angiosperms (Doyle 2005). This showed that molecular data refute older assumptions that the first angiosperms had a pollen wall (exine) with granular structure, as in several gymnosperm groups, which would have meant that the first angiosperm pollen would be difficult to distinguish from gymnosperm pollen in the fossil record. Instead, the most basal living lines have columellar structure, as in most other angiosperms, implying that the first known pollen with such structure in the Early Cretaceous may be closer in time to the origin of angiosperms than previously assumed. As part of my continuing work on phylogeny, evolution, and biogeography of the tropical family Annonaceae (which include cherimoyas and pawpaws), my former student Tanya Scharaschkin (Queensland University of Technology, Brisbane) and I published an analysis of phylogeny and biogeography of Anaxagorea, the most basal evolutionary line in Annonaceae (Scharaschkin and Doyle 2005). Previous work had suggested that Anaxagorea might be of Northern Hemisphere (Laurasian) origin, since it is the only genus of Annonaceae with a disjunct distribution in Asia and tropical America. However, our analyses indicate that the most basal species are South American, supporting a Southern Hemisphere (Gondwanan) origin for both Anaxagorea and Annonaceae as a whole. During a six-month sabbatical based in New Zealand, I was able to observe several critical primitive angiosperm groups in their natural habitats in New Zealand, Australia, and New Caledonia. These include Amborella, the earliest diverging line in all angiosperms, Austrobaileya, Ascarina (Chloranthaceae, a family in which I have a long-standing interest), and many genera in the more derived orders Magnoliales (Eupomatia, Galbulimima), Winteraceae (Tasmannia, Bubbia, Pseudowintera), and Laurales (Hedycarya, Laurelia, Atherosperma). Besides providing a large number of photos for future courses and scientific talks, this gave me direct experience with the habitat preferences and ecology of these plants. I also completed two papers scheduled to appear in 2006: on morphological evolution in Anaxagorea (with Scharaschkin) and on phylogeny of living and fossil seed plants and the origin of angiosperms.

Impacts
Angiosperms are the dominant plants in modern terrestrial ecosystems and the basis of almost all human agriculture. Improved understanding of their origin and diversification may have practical impacts through the new insights it provides on plant genetics, pollination biology, and development of flowers and fruits. Better understanding of the evolution of flowers, fruits, seeds, and pollen in primitive angiosperms may have practical value in genetic engineering and improvement of yields in traditional and new crop species, especially in tropical families such as Annonaceae, in which cherimoya is already a significant fruit crop and other genera are under investigation for agricultural use. Many living primitive angiosperms are members of restricted and threatened plant communities in the tropics and subtropics, and efforts to conserve them may also be of value in preservation and sustainable use of their endangered habitats and plant and animal associates.

Publications

  • Doyle, J.A. 2005. Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44: 227-251.
  • Scharaschkin, T. and J.A. Doyle. 2005. Phylogeny and historical biogeography of Anaxagorea (Annonaceae) using morphology and non-coding chloroplast sequence data. Systematic Botany 30: 712-735.


Progress 01/01/04 to 12/31/04

Outputs
This project focuses on reconstruction of evolutionary relationships among living primitive angiosperms (flowering plants) and the oldest fossil angiosperms from Cretaceous sediments, based on cladistic analyses of morphological and molecular data. I have continued to collaborate with Peter Endress (Zurich) on a book-length study of primitive angiosperms, including a survey of morphological characters from all parts of the plant, which should be a basic resource in the present revival of interest in plant morphology and development in an evolutionary framework ("evo-devo"). We completely revised our treatment of floral characters in the light of another recently published survey and reappraised pollen characters for a talk on pollen evolution in angiosperms that I presented at the International Palynological Congress in Granada (submitted). I continued to publish results of a collaboration with Annick Le Thomas (Paris), Herve Sauquet (Stockholm), and Tanya Scharaschkin (Brisbane) on phylogeny of the related tropical families Myristicaceae (including the crop tree nutmeg) and Annonaceae (including cherimoyas and pawpaws), with a paper on biogeography of these families (Doyle et al. 2004). Although relationships within Myristicaceae and Annonaceae suggest that they had similar geographic histories - origin in Africa-South America, followed by migration into Asia, consistent with the Late Cretaceous age of Annonaceae inferred from fossil and molecular data - DNA sequence divergence in Myristicaceae is much lower, implying either recent dispersal across ocean barriers or more likely a major slowdown in molecular evolution. With Helena Eklund (Uppsala) and Patrick Herendeen (George Washington University), I completed a detailed morphological phylogenetic analysis of Chloranthaceae (which include the house plant Chloranthus spicatus), one of the first living angiosperm families recognized in the fossil record (Eklund et al. 2004). These results show that morphological data on relationships in the family are generally consistent with molecular data, contrary to earlier indications. They also show that some Cretaceous fossils are related to but more primitive than the living genera Hedyosmum and Chloranthus, whereas others represent extinct lines more primitive than the whole family or located between living genera. Feild et al. (2004) synthesized diverse evidence on the ecology of the first angiosperms. Contrary to older ideas that the first angiosperms were trees of stable forests, fast-growing shrubs of disturbed semiarid habitats, or aquatics, ecophysiological studies of living groups now placed at the base of the evolutionary tree of angiosperms and reappraisal of fossil evidence suggest that the first angiosperms were adapted to dark and disturbed habitats of the forest understory. Our results also suggest that the high speciation rates considered typical of angiosperms did not evolve until angiosperms became more sun-tolerant and "broke out" of their ancestral habitats.

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all human agriculture. Improved understanding of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Better understanding of the evolution of flowers, fruits, and seeds may eventually be of practical use in genetic engineering. Recognition of very different rates of natural molecular evolution of the sort inferred in the related families Myristicaceae and Annonaceae may affect our views on the prospects for genetic modification of different plant groups. Better understanding of the constraints on evolution of ecological traits in a phylogenetic context, as promoted by studies such as Feild et al. (2004), may also help in engineering or selecting ecophysiological features in both traditional and new crop plant species.

Publications

  • Doyle, J.A., H. Sauquet, T. Scharaschkin, and A. Le Thomas, A. 2004. Phylogeny, molecular and fossil dating, and biogeographic history of Annonaceae and Myristicaceae (Magnoliales). International Journal of Plant Sciences 165 (4 Supplement) S55-S67.
  • Eklund, H., J.A. Doyle, and P.S. Herendeen. 2004. Morphological phylogenetic analysis of living and fossil Chloranthaceae. International Journal of Plant Sciences 165: 107-151.
  • Feild, T.S., N.C. Arens, J.A. Doyle, T.E. Dawson, and M.J. Donoghue. 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30: 82-107.
  • Groot, E.P., J.A. Doyle, S.A. Nichol, and T.L. Rost. 2004. Phylogenetic distribution and evolution of root apical meristem organization in dicotyledonous angiosperms. International Journal of Plant Sciences 165: 97-105.


Progress 01/01/03 to 12/31/03

Outputs
This project focuses on reconstruction of evolutionary relationships among living primitive angiosperms (flowering plants), based on cladistic analyses of morphological and molecular data, and the evolutionary implications of the earliest fossil angiosperms from Cretaceous sediments. I have continued to collaborate with Peter Endress (University of Zurich) on a book-length study of the phylogeny of primitive angiosperms as a whole, including a critical survey of morphological characters from all parts of the plant, which should be a basic resource in the present revival of interest in plant morphology in a phylogenetic framework, including evolutionary and developmental studies (evo-devo) of both wild and crop plants. A collaboration with Herve Sauquet (University of Paris) on phylogeny of the family Myristicaceae, which includes the tropical crop tree nutmeg, is essentially completed. Our main paper, on morphological and molecular analyses and their implications for the evolution of morphological characters (Sauquet et al., 2003), indicates that the Madagascar genus Mauloutchia, previously thought to be primitive because of its free rather than fused anthers, is actually derived, but it confirms the older view that Asian genera (including Myristica, nutmeg) are also derived. Another paper, on biogeography of Myristicaceae and the related family Annonaceae, has been accepted. Although inferred phylogenetic relationships within Myristicaceae and Annonaceae imply that they had similar geographic histories - origin in Africa-South America, later migration into Asia, consistent with the Late Cretaceous age of Annonaceae inferred from fossil and molecular data - DNA sequence divergence in Myristicaceae is markedly lower, implying either implausibly recent dispersal across ocean barriers or more likely a major slowdown in molecular evolution. With Helena Eklund (Uppsala) and Patrick Herendeen (George Washington University), I completed a detailed morphological phylogenetic analysis of Chloranthaceae (including the house plant Chloranthus spicatus), one of the first living angiosperm families recognized in the fossil record, aimed at establishing the position of fossil pollen and flowers in the phylogeny of the modern species. An article on the implications of this analysis for evolution of the remarkably simple flowers of Chloranthaceae is now published (Doyle et al. 2003), and the analysis itself is in press. Our results place Cretaceous fossils that resemble Chloranthus but differ in having three free stamens rather than a three-lobed androecium below the living genus, supporting the hypothesis that the modern androecium originated by fusion of three stamens, whereas fossil flowers and pollen compared with the genus Ascarina represent a more distantly related extinct lineage. Friis et al. (2003) argued that Archaefructus, an aquatic fossil plant described from the Lower Cretaceous of China and interpreted as more primitive than all living angiosperms, may instead be a specialized early line with flowers reduced for an aquatic habitat.

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all agriculture. Improved understanding of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Understanding of the evolution of flowers, fruits, and seeds may eventually be of use in genetic engineering.

Publications

  • Doyle, J.A., H. Eklund and P.S. Herendeen. 2003. Floral evolution in Chloranthaceae: implications of a morphological phylogenetic analysis. International Journal of Plant Sciences 164(Supplement):S365-S382.
  • Friis, E.M., J.A. Doyle, P.K. Endress and Q. Leng. 2003. Archaefructus - angiosperm precursor or specialized early angiosperm? Trends in Plant Science 8:369-373.
  • Sauquet, H., J.A. Doyle, T. Scharaschkin, T. Borsch, K.W. Hilu, L.W. Chatrou and A. Le Thomas. 2003. Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution. Botanical Journal of the Linnean Society 142:125-186.


Progress 01/01/02 to 12/31/02

Outputs
This project focuses on phylogenetic (cladistic) analysis of evolutionary relationships among living primitive angiosperms (flowering plants), based on morphological and molecular data, and the evolutionary implications of the oldest definite fossil pollen of angiosperms from Cretaceous sediments. In 2002 I published a general review of this topic (dated 2001), emphasizing agreements between the Cretaceous fossil record of angiosperms and molecular phylogenies (the earliest fossils appear related to lines placed near the base of the angiosperms in molecular phylogenetic trees, whereas lines placed higher appear later) and the necessity of reorienting the search for angiosperm relatives toward fossil taxa, because molecular data have refuted the earlier view that angiosperms are related to living Gnetales. I collaborated with Peter Endress (University of Zurich) on a phylogenetic analysis of primitive angiosperms as a whole, for a book series published by the Smithsonian Institution. We have defined and scored most characters for this analysis and are writing discussions on the definition of both floral and vegetative characters. This should be a basic resource in the present revival of interest in plant morphology in a phylogenetic framework, as background for studies on evolution and development (evo-devo) of both wild and crop plants. A collaboration with Herve Sauquet (University of Paris) on phylogeny of the family Myristicaceae is nearly completed. Our main paper has been accepted for publication (Sauquet et al., in press). Our results imply that the Malagasy genus Mauloutchia, previously thought to be primitive because of its free anthers (versus fused in other Myristicaceae), is actually derived, but they confirm the older view that Asian groups (including Myristica, nutmeg) are derived. At a symposium on biogeography (Doyle et al., 2002), we showed that our phylogenetic trees imply that Myristicaceae and the related family Annonaceae had similar geographic histories: origin in Africa-South America, later migration into Asia. This scenario is consistent with the Late Cretaceous and Tertiary fossil record of Annonaceae and molecular estimates of their age, but DNA sequence divergence in Myristicaceae is markedly lower, implying either implausibly recent dispersal across ocean barriers or more likely a major slowdown in molecular evolution. Another project, with Helena Eklund (University of Leeds) and Patrick Herendeen (George Washington University), is a morphological phylogenetic analysis of the family Chloranthaceae, one of the first living groups to appear in the fossil record. At a symposium in Zurich (Doyle et al., 2002) we presented implications of this analysis for evolution of the remarkably simple flowers of Chloranthaceae, and we are currently writing up the analysis itself. Our results suggest where fossil pollen and flowers fit in the phylogeny of living Chloranthaceae. They imply that Late Cretaceous fossils resembling Chloranthus are more primitive than the living genus and support the hypothesis that its bizarre and controversial three-lobed androecium originated by fusion of three stamens.

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all agriculture. Improved understanding of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Understanding of the evolution of flowers, fruits, and seeds may eventually be of use in genetic engineering.

Publications

  • Doyle, J.A. 2001. Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms. Palaeobotanist 50:167-188.
  • Doyle, J.A., H. Eklund and P.S. Rendeen. 2002. Phylogenetic analysis and floral evolution in Chloranthaceae. Flowers: Diversity, Development & Evolution (University of Zurich), Program and Abstracts, p. 18.
  • Doyle, J.A., J. Sauquet, T. Scharaschkin and A. Le Thomas. 2002. Phylogeny, molecular and fossil dating, and biogeographic history of Magnoliales - contrasts between Annonaceae and Myristicaceae. Botany 2002 (Madison, Wisconsin), Abstracts, p. 176.
  • Sauquet, H., J.A. Doyle, T. Scharaschkin, T. Borsch, K.W. Hilu, L.W. Chatrou and A. Le Thomas. 2003. Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution. Botanical Journal of the Linnean Society. In Press.


Progress 01/01/01 to 12/31/01

Outputs
This project focuses on phylogenetic (cladistic) analysis of evolutionary relationships among living primitive angiosperms (flowering plants) based on morphological characters and molecular data, analysis of relationships within families of primitive angiosperms, and evolutionary implications of the oldest definite fossil pollen of angiosperms from Cretaceous sediments. Sanderson and Doyle (2001) explores conflicts between estimates of the age of the angiosperms based on the fossil record (which indicates that angiosperms began to diversify in the Early Cretaceous, about 130 million years ago) and molecular data (which have given ages up to 320 million years, by assuming a constant rate of molecular evolution, or molecular clock). Based on analyses of rbcL and 18S ribosomal DNA sequences, we show that molecular dates can be biased by unequal rates of molecular evolution in different lines, different assumptions on relationships within angiosperms, and different rates of evolution at different sites in the DNA. Our results confirm earlier indications that herbaceous groups, such as grasses, legumes, and Solanaceae, which include many crop plants, have accelerated rates of molecular evolution, and their use as exemplars of the angiosperms may have contributed to age estimates that are too old. This study is continuing with tests of the implications of new gene sequences and new methods of analysis (Doyle et al. 2001). I have continued to collaborate with Peter Endress (University of Zurich) on a phylogenetic analysis of primitive angiosperms as a whole, aimed at expanding a paper we published in 2000 into a book for a series published by the Smithsonian Institution. So far we have redefined flower and inflorescence characters in light of more recent studies. I have also begun a project with Herve Sauquet (University of Paris) on phylogeny of the primitive angiosperm family Myristicaceae, which includes the tropical crop tree nutmeg, based on morphology and DNA sequences. This uses new morphological observations and data amassed in previous studies of primitive angiosperms (with Endress) and the related family Annonaceae (with Le Thomas). We presented preliminary results at a meeting of the Botanical Society of America (Sauquet et al. 2001). Most significant is the conclusion that the Madagascan genus Mauloutchia, previously thought to be most primitive because of its numerous free (rather than fused) anthers, is more advanced than assumed, but it belongs to a group of Madagascan and African genera that may be basal. Another new collaboration on living primitive angiosperms, with Helena Eklund (University of Leeds) and Patrick Herendeen (George Washington University), is a morphological phylogenetic analysis of the family Chloranthaceae (including the house plant CHLORANTHUS SPICATUS), which is one of the first living groups to appear in the Cretaceous fossil record. Our results promise to place early fossil pollen and flowers more accurately in the context of living members.

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all agriculture. Improved understanding of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Understanding of the evolution of flowers, fruits, and seeds may eventually be of use in genetic engineering.

Publications

  • Sanderson, M.J. and Doyle, J.A. 2001. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Am. J. Bot. 88:1499-1516.
  • Doyle, J.A., Sanderson, M.J. and Magallon, S. 2001. Integrating fossil and molecular data on the age of angiosperms: effects of fossil age constraints and rate smoothing methods. Botany 2001 (Albuquerque, New Mexico) Abstracts, p. 63.
  • Sauquet, H., Le Thomas, A., Doyle, J.A., Hilu, K.H., Borsch, T. and Chatrou, L.W. 2001. Insights into the origin and evolution of Myristicaceae (Magnoliales), based on morphological and molecular data. Botany 2001 (Albuquerque, New Mexico) Abstracts, p. 140.


Progress 01/01/00 to 12/31/00

Outputs
This project focuses on phylogenetic (cladistic) analysis of evolutionary relationships among living primitive angiosperms (flowering plants) based on morphological characters and molecular data, analysis of relationships within families of primitive angiosperms, and evolutionary implications of the oldest definite fossil pollen of angiosperms from Cretaceous sediments. Donoghue and Doyle (2000) reviewed recent molecular phylogenetic analyses based on multiple genes that indicate that Gnetales, which morphological cladistic analyses identify as the closest living relatives of angiosperms, are instead related to conifers, and explored implications for the evolution of morphological characters. Doyle (2000) synthesized evidence from phylogenetic analyses and the fossil record on relationships and geographic history of the Southern Hemisphere primitive angiosperm family Winteraceae, famous for its vesselless wood. The stem-lineage leading to Winteraceae apparently separated from its sister family Canellaceae in the Early Cretaceous in the African-South American tropics, while the crown-group including all the living members was derived from a line that migrated into Southern Gondwana (now fragmented into South Africa, Madagascar, Australasia, and South America). This may fit phylogenetic inferences that vessels were present in the ancestors of Winteraceae but were lost as a consequence of migration into cooler climates. Doyle and Endress (2000) presented cladistic analyses of primitive angiosperms ("Magnoliidae," basal monocots, eudicots) based on a new morphological data set and published DNA sequences of rbcL, 18S rDNA, and atpB. Analysis of the new morphological data showed many shifts toward relationships inferred from molecular data (separation of Illiciales from Winteraceae; separation of AMBORELLA, AUSTROBAILEYA, Trimeniaceae, and Chloranthaceae from Laurales; association of Winteraceae and Canellaceae), but also continued conflicts (association of monocots with Nymphaeales). Trees based on all data combined generally agreed with molecular trees but suggested new resolutions of relationships that were ambiguous based on molecular data alone (placement of Chloranthaceae just above the first three lines; association of monocots with Piperales, Lauraceae with Hernandiaceae). This study indicated that vesselless wood, two-trace nodes, columellar pollen structure, and ascidiate carpels sealed by secretion are ancestral. Doyle, Bygrave and Le Thomas (2000) compared and combined a previously published morphological data set on Annonaceae, the largest family of living primitive angiosperms, with rbcL sequences of Bygrave. This study confirmed many morphological results (basal position of ANAXAGOREA, unity of groups with inaperturate pollen) but refuted others (the "xylopioid" clade). Critical reexamination suggested that pollen and stamen characters that united the xylopioids were incorrectly interpreted. Seed characters appear to be more reliable than vegetative, floral, and pollen characters.

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all agriculture. Improved understanding of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Understanding of the evolution of flowers, fruits, and seeds may eventually be of use in genetic engineering.

Publications

  • Donoghue, M.J. and Doyle, J.A. 2000. Seed plant phylogeny: demise of the anthophyte hypothesis? Curr. Biol. 10:R106-R109.


Progress 01/01/99 to 12/31/99

Outputs
This project focuses on phylogenetic (cladistic) analysis of evolutionary relationships among living primitive angiosperms (flowering plants), using morphological characters, and integration of morphological and molecular data; reconstruction of relationships within families of primitive angiosperms; and fossil pollen of the oldest definite angiosperms from Cretaceous sediments and its implications for early angiosperm evolution. Toward the first goal, Doyle & Endress (1999) presented a cladistic analysis of primitive angiosperms ("Magnoliidae" and basal members of monocots and eudicots), in which we amassed morphological characters from the literature and our own observations of living and preserved material, and combined these data with DNA sequences of three genes (rbcL, 18S rDNA, atpB), provided by P. S. Soltis (Washington State University). Apparently as a result of improved morphological data, phylogenetic trees based on this new data set showed many shifts in the direction of trees based on molecular data (separation of Illiciales from Winteraceae; separation of AMBORELLA, AUSTROBAILEYA, Trimeniaceae, and Chloranthaceae from Laurales; relationship of Winteraceae and Canellaceae), but also continued conflicts (association of Nymphaeales and monocots). The combined analyses generally agreed with molecular results but suggested new resolutions of relationships that were ambiguous based on molecular data alone (placement of Chloranthaceae just above the first three lines; relationship of monocots with Piperales). This study confirmed the primitive status of several controversial characters, such as vessel less wood, two-trace nodes, columellar pollen wall structure, and ascidiate carpels sealed by secretion. Doyle (1999a) was a commentary on a Russian article by A. S. Antonov, which was intended to convince Russian botanists of the value of molecular systematics. This commentary continued the exploration of the significance of conflicts and agreements between morphological and molecular data, arguing that conclusions based on the two sorts of data usually converge when they are both analyzed with appropriate cladistic methods and complement each other in cases of ambiguity. Doyle (1999b) synthesized the African Early Cretaceous fossil record of angiosperm pollen types that can be associated with living groups, showing the early appearance of several surviving primitive angiosperm lines, the southward migration of taxa such as Winteraceae and Proteaceae from the tropics to the south temperate zone, and the fact that several lines documented in Africa in the Early Cretaceous now survive as relicts in Madagascar (Winteraceae, Chloranthaceae, Didymelaceae).

Impacts
Angiosperms are the dominant group of plants in the modern world and the basis of almost all agriculture. An improved picture of their origin and diversification may have practical impacts on plant genetics, pollination biology, and morphology and development of flowers and fruits. Understanding of the evolution of flowers, fruits, and seeds may eventually be of use in genetic engineering.

Publications

  • Doyle, J.A. 1999. Plant molecular systematics, classical systematics, and morphological cladistics comments on the article by A. S. Antonov. Zh. Obshch. Biol. 60344-351.
  • Doyle, J.A. 1999. The rise of angiosperms as seen in the African Cretaceous pollen record. Palaeoecol. Africa 263-30.
  • Doyle, J.A., and Endress, P.K. 1999. Morphological cladistic analyses of basal angiosperms. XVI Internat. Bot. Congr. Abstr. 89.


Progress 01/01/98 to 12/01/98

Outputs
This project focuses on (1) the origin of angiosperms in the context of evolutionary relationships (phylogeny) among seed plants as a whole and (2) relationships among primitive angiosperms. Doyle (1998a) analyzes conflicts between morphological and molecular data on seed plant phylogeny: it presents statistical evidence that molecular analyses are correct where they have given consistent results but morphological analyses are equivocal (that both angiosperms and Gnetales are natural groups), and vice versa (that angiosperms and Gnetales are related to each other). Doyle (1998b) reviews morphological and molecular phylogenetic analyses of vascular plants as a whole, stressing where these analyses resolve long-standing problems and where more work is needed. Doyle, Bygrave & Le Thomas (1998) presents initial results of comparing and combining previously published morphological data from this project on phylogeny of Annonaceae, the largest family of living primitive angiosperms, with new molecular data (rbcL); this confirms many morphological results (basal position of ANAXAGOREA, unity of groups with inaperturate and tetrad pollen), but refutes others (association of CANANGA, XYLOPIA, and NEOSTENANTHERA). Critical examination indicates that pollen and stamen characters that appeared to support the latter relationship were incorrectly interpreted, while seed characters were most reliable.

Impacts
(N/A)

Publications

  • DOYLE, J.A. 1998a. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Mol. Phylog. Evol.
  • DOYLE, J.A. 1998b. Phylogeny of vascular plants. Annu. Rev. Ecol. Syst. 29:567-599.
  • DOYLE, J.A., BYGRAVE, P. and LE THOMAS, A. 1998. Implications of molecular data for pollen evolution in Annonaceae. Pollen and Spores 1998, Morphology and Biology (Royal Botanic Gardens, Kew), Abstracts,


Progress 01/01/97 to 12/01/97

Outputs
This project focuses on (1) the origin of angiosperms in the context of evolutionary relationships (phylogeny) of seed plants as a whole and (2) relationships among primitive angiosperms. In a study on the use of molecular data to estimate the age of angiosperms, Doyle & Sanderson (1997) suggested that previous estimates, some of which were much older than the oldest angiosperm fossils, were too old because of incorrect assumptions on seed plant phylogeny, limitations of molecular data in reconstructing ancient radiations, and effects of groups such as grasses with high rates of molecular evolution. To test the relative importance of pollen and other characters in reconstructing phylogeny of Annonaceae, the largest family of living primitive angiosperms, Doyle & Le Thomas (1997a) analyzed our previously published data set with pollen characters removed: the results suggest that pollen is especially important in establishing which groups are at the base of the family, a conclusion confirmed by molecular data. Le Thomas & Doyle (1996) and Doyle & Le Thomas (1997b) discussed implications for the geographic history of Annonaceae, concluding that the basal split into ANAXAGOREA and other genera represents a split into northern (Laurasian) and southern (Gondwanan) lines, and that diversification of the latter occurred in Africa and South America, followed by migration into Asia and Australia.

Impacts
(N/A)

Publications

  • LE THOMAS, A. and DOYLE, J.A. 1996. Implications d'une analyse cladistique dans l'histoire geographique des Annonaceae: famille d'Angiospermes primitives, pp. 171-180. IN J.-L. Guillaumet, M. Belin and H. Puig (Eds.), PHYTOGEOGRAPHIE TROP.
  • DOYLE, J.A. and LE THOMAS, A. 1997a. Significance of palynology for phylogeny of Annonaceae: experiments with removal of pollen characters. Plant Systematics and Evolution 206:133-159.
  • DOYLE, J.A. and LE THOMAS, A. 1997b. Phylogeny and geographic history of Annonaceae. Geographie Physique et Quaternaire 51:355-363.
  • DOYLE, J.A. and SANDERSON, M.J. 1997. Fossils, molecular clocks, and the age of angiosperms. American Journal of Botany 84 (6,


Progress 01/01/96 to 12/30/96

Outputs
One goal of this project is to clarify the origin of angiosperms by analyzing relationships among seed plants as a whole. Doyle (1996) completed a seed plant analysis begun in 1995, which indicates that angiosperms and related plants (fossil Bennettitales and CAYTONIA, living Gnetales) are derived from Permian glossopterids, which had fertile structures that provide a prototype for angiosperm carpels containing ovules with two integuments. Doyle & Gensel (1996) synthesized spore and pollen characters across all green plants: a literature survey revealed a major change in development of the pollen wall (exine) between "lower" groups and seed plants and reaffirmed the controversial homology of the inner layer (endexine) in gymnosperms and angiosperms. In the part of this project devoted to relationships among living primitive angiosperms, Le Thomas & Doyle (1996) discussed implications of their previous analyses of the large family Annonaceae for relationships of those members found in Madagascar, raising the possibility that Madagascar served as a bridge for migration of African lines into Asia during the Tertiary Period. Doyle & Le Thomas (1996) documented and analyzed a significantly improved data set for Annonaceae and discussed in detail the implications of the phylogenetic trees obtained for evolution of characters, showing particularly informative trends in pollen and seed features.

Impacts
(N/A)

Publications

  • DOYLE, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157(6, Supplement):S3-S39.
  • DOYLE, J. A. and GENSEL, P. G. 1996. Phylogenetic characters in land plant spores and pollen. American Journal of Botany 83(6, Supplement):107.
  • LE THOMAS, A. and DOYLE, J. A. 1996. Geographic relationships of Malagasy Annonaceae, pp. 85-94. IN W. R. Lourenco (Ed.), Biogeographie de Madagascar, Editions de l'ORSTOM, Paris.
  • DOYLE, J. A. and LE THOMAS, A. 1996. Phylogenetic analysis and character evolution in Annonaceae. Bulletin du Museum National d'Histoire Naturelle, section B, Adansonia. 18:111-166.


Progress 01/01/95 to 12/30/95

Outputs
One goal of this project is elucidating the origin of angiosperms through phylogenetic analysis of seed plants as a whole. I conducted a new analysis for a symposium on Gnetales (Doyle, 1995a), the closest living relatives of angiosperms, using recently published data on fossils and new characters from two other seed plant analyses. This refutes the conclusion of one analysis that angiosperms are derived from Gnetales and implies instead that both taxa, plus fossil Bennettitales, PENTOXYLON, and CAYTONIA, are related to the Permian glossopterids of Gondwana. This confirms the view that angiosperm ovules are derived from cupules like those of glossopterids or CAYTONIA, the carpel from the leaf-like structure on which the cupules were borne. In a related analysis (Doyle, 1995b), I tested the significance of pre-Cretaceous fossils that may be angiosperm relatives: this supports views that the first angiosperms were semi-herbaceous plants rather than MAGNOLIA-like trees. Another goal is reconstructing the evolution of Annonaceae, the largest family of living primitive angiosperms. We published a new phylogenetic analysis of the family (Doyle & Le Thomas, 1995), adding two African genera not included previously, which implies that groups with single inaperturate pollen grains were derived from ancestors with tetrad pollen, a result supported by independent molecular studies.

Impacts
(N/A)

Publications