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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Page viii Cite
Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
×
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
×
PageR9
Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
×
PageR10
Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
×
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Suggested Citation:"Front Matter." National Academy of Sciences. 2000. Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins. Washington, DC: The National Academies Press. doi: 10.17226/9766.
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Variation and Evolution in Plants and Microorganisms TOWARD A NEW SYNTHESIS 50 YEARS AFTER STEBBINS Francisco J. Ayala, Walter M. Fitch, and Michael T. Clegg, Editors NATIONAL ACADEMY PRESS Washington, D.C.

NATIONAL ACADEMY PRESS • 2101 Constitution Avenue, N.W. • Washington, D.C. 20418 This volume is based on the National Academy of Sciences’ Colloquium on the Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years after Stebbins. The articles appearing in these pages were contributed by speakers at the collo- quium and have not been independently reviewed. Any opinions, findings, conclusions, or recommendations expressed in this volume are those of the authors and do not necessarily reflect the views of the National Academy of Sciences. Library of Congress Cataloging-in-Publication Data Variation and evolution in plants and microorganisms : toward a new synthesis 50 years after Stebbins / Francisco J. Ayala, Walter M. Fitch, and Michael T. Clegg, editors. p. cm. Includes bibliographical references and index. ISBN 0-309-07075-9 (hardcover) — ISBN 0-309-07099-6 (pbk.) 1. Plants—Evolution—Congresses. 2. Plants—Variation—Congresses. I. Ayala, Francisco José, 1934- II. Fitch, Walter M., 1929- III. Clegg, Michael T., 1941- IV. Colloquium on the Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins (2000 : Beckman Center of the National Academies) QK980 .V37 2000 581.3'8--dc21 00-010861 Additional copies of this report are available from National Academy Press, 2101 Constitu- tion Avenue, N.W., Lockbox 285, Washington, D.C. 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu Copyright 2000 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

National Academy of Sciences National Academy of Engineering Institute of Medicine National Research Council The National Academy of Sciences is a private, nonprofit, self-perpetuating soci- ety of distinguished scholars engaged in scientific and engineering research, dedi- cated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Bruce M. Alberts is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its mem- bers, sharing with the National Academy of Sciences the responsibility for advis- ing the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. William A. Wulf is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Kenneth I. Shine is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sci- ences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal gov- ernment. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in pro- viding services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. William A. Wulf are chairman and vice chairman, respectively, of the National Research Council.

Preface “T he present book is intended as a progress report on [the] synthetic approach to evolution as it applies to the plant kingdom” (Stebbins, 1950, p. ix). With this simple statement, G. Ledyard Stebbins formulated the objectives of Variation and Evolution in Plants (Stebbins, 1950), published in 1950, the last of a quartet of classics that, in the second quarter of the twentieth century, set forth what became known as the “synthetic theory of evolution” or “the modern synthesis.” The other books are Theodosius Dobzhansky’s Genetics and the Origin of Species (1937), Ernst Mayr’s Systematics and the Origin of Species (1942) and George Gaylord Simpson’s Tempo and Mode in Evolution (1944). The per- vading conceit of these books is the molding of Darwin’s evolution by natural selection within the framework of rapidly advancing genetic knowledge. Stebbins said it simply: “In brief, evolution is here visualized as primarily the resultant of the interaction of environmental variation and the genetic variability recurring in the evolving population” (Stebbins, 1950, p. xi). Variation and Evolution in Plants distinctively extends the scope of the other books to the world of plants, as explicitly set in the book’s title. Dobzhansky’s perspective had been that of the geneticist and he set the tone for the others, Mayr’s that of the zoologist and systematist, and Simpson’s that of the paleobiologist. All four books were outcomes of the famed Jesup Lectures at Columbia University. Plants, with their unique genetic, physiological and evolutionary features, had all but been left completely out of the synthesis until that point. In 1941, the eminent v

vi / Preface botanist Edgar Anderson, had been invited to write botany’s analogue to Mayr’s Systematics and the Origin of the Species and to publish it jointly with Mayr’s book. Anderson did not fulfill the task, and Stebbins was thereafter invited to deliver the Jesup Lectures in 1947. Variation and Evo- lution in Plants is the outgrowth of the Lectures. The mathematical underpinnings of the modern synthesis were set between 1918 and 1931 by R. A. Fisher (1930) and J.B.S. Haldane (1932) in Britain, and Sewall Wright (1931) in the United States. According to Dar- win, evolutionary change occurs by natural selection of small individual differences appearing every generation within any species. Any change effected by selection is typically small but they amount to major change over time. Thomas Huxley and Francis Galton, among Darwin’s most dedicated supporters, argued instead that evolution occurs by selection of discontinuous variations, or sports; evolution proceeds rapidly by dis- crete leaps. Natural selection operating only upon gradual differences among individuals, could hardly account, in Huxley’s view, for the gaps between existing species evident in the paleontological record. According to Galton, evolution proceeds by “jerks,” some of which imply consider- able organic change, rather than as a smooth and uniform process. In the latter part of the nineteenth century, the biometricians Karl Pearson and W.F.R. Weldon believed, like Darwin, in the primary impor- tance of common individual differences. Like other geneticists, William Bateson argued, rather, for the primary importance of discontinuous vari- ations. The controversy was acrimonious. The rediscovery of Mendelian inheritance in 1900 might have served as the common grounds to resolve the conflict. Instead, the dispute between biometricians and geneticists extended to continental Europe and to the United States. Bateson was the champion of the Mendelians, many of whom accepted the mutation theory proposed by De Vries (1900), and denied that natural selection played a major role in evolution. The biometricians for their part argued that Men- delian characters were sports of little significance for the evolutionary process. Fisher, Haldane, and Wright advanced theoretical models of evo- lutionary processes based on the natural selection of genetic changes (mu- tations) that are individually small, but are cumulatively of great conse- quence. Theodosius Dobzhansky first and, then, Mayr, Simpson, and Stebbins (and, less notably, many others) completed the mathematicians’ theoreti- cal propositions with a wealth of biological knowledge and empirical support. Stebbins was particularly suited to bring in the evidence from plants. He was born in 1906 and had become interested in natural history from childhood. He started botanizing in his early teens while a student at Cate School in Santa Barbara (California). As an undergraduate at Harvard (1924–1928) he came under the influence of Merritt Lyndon Fer-

Preface / vii nald (1873–1950), a charismatic teacher and distinguished botanist, whom Stebbins accompanied on field trips to study the New England flora. In 1928, Stebbins became a graduate student at Harvard and worked on the cytology, geographic variation, and seed development of Antennaria, a genus that bore several apomictic species that could be collected in nearby localities. The distinctive evolutionary role of vegetative reproduction in plants would remain a focus of interest to the end of his life. The 17 papers that follow were presented at a colloquium sponsored by the National Academy of Sciences, “Variation and Evolution in Plants and Microorganisms. Towards a New Synthesis 50 Years after Stebbins.” The colloquium, held at the Beckman Center of the National Academies, in Irvine, California, January 27–29, 2000, sought to celebrate the 50th anniversary of the publication of Stebbins’ classic. Professor Stebbins, although frail for the last few years, intended to attend the colloquium. Alas, he became ill around Christmas time and died on January 19, 2000, a few days before the colloquium was held, just about two weeks after his 94th birthday, on January 6. The “Appreciation” (Chapter 1) was read by Peter Raven, after dinner on January 28th, at the time and place that had been reserved for Stebbins’ own words. The 16 papers following the “Ap- preciation” are organized into five successive sections: Early Evolution and the Origin of Cells, Virus and Bacterial Models, Protoctist Models, Population Variation, Trends and Patterns in Plant Evolution. We are grateful to the National Academy of Sciences for the generous grant that financed the colloquium, to the staff of the Arnold and Mabel Beckman Center for their skill and generous assistance, and to Mrs. Denise Chilcote, who performed the administrative functions of the colloquium with skill and dedication. REFERENCES De Vries, H. (1900) Sur les unités des caractères spécifiques et leur application á l’étude des hybrides. Rev. Gen. Bot. 12, 257–271. Dobzhansky, Th. (1937) Genetics and the Origin of Species (Columbia University Press, New York); 2nd Ed., 1941; 3rd Ed., 1951. Fisher, R. A. (1930) The Genetical Theory of Natural Selection (Clarendon, Oxford). Haldane, J. B. S. (1932) The Causes of Evolution (Harper, New York). Mayr, E. (1942) Systematics and the Origin of Species (Columbia University Press, New York). Simpson, G. G. (1944) Tempo and Mode in Evolution (Columbia University Press, New York). Stebbins, G. L. (1950) Variation and Evolution in Plants (Columbia University Press, New York). Wright, S. (1931) Evolution in mendelian populations. Genetics 16, 97–159.

Contents PART I: EARLY EVOLUTION AND THE ORIGIN OF CELLS 1. G. Ledyard Stebbins (1906–2000)—An Appreciation 3 Peter H. Raven 2. Solution to Darwin’s Dilemma: Discovery of the Missing Precambrian Record of Life 6 J. William Schopf 3. The Chimeric Eukaryote: Origin of the Nucleus from the Karyomastigont in Amitochondriate Protists 21 Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero 4. Dynamic Evolution of Plant Mitochondrial Genomes: Mobile Genes and Introns and Highly Variable Mutation Rates 35 Jeffery D. Palmer, Keith L. Adams, Yangrae Cho, Christopher L. Parkinson, Yin-Long Qiu, and Keming Song PART II: VIRAL AND BACTERIAL MODELS 5. The Evolution of RNA Viruses: A Population Genetics View 61 Andrés Moya, Santiago E. Elena, Alma Bracho, Rosario Miralles, and Eladio Barrio ix

x / Contents 6. Effects of Passage History and Sampling Bias on Phylogenetic Reconstruction of Human Influenza A Evolution 83 Robin M. Bush, Catherine B. Smith, Nancy J. Cox, and Walter M. Fitch 7. Bacteria are Different: Observations, Interpretations, Speculations, and Opinions About the Mechanisms of Adaptive Evolution in Prokaryotes 99 Bruce R. Levin and Carl T. Bergstrom PART III: PROTOCTIST MODELS 8. Evolution of RNA Editing in Trypanosome Mitochondria 117 Larry Simpson, Otavio H. Thiemann, Nicholas J. Savill, Juan D. Alfonzo, and D.A. Maslov 9. Population Structure and Recent Evolution of Plasmodium falciparum 143 Stephen M. Rich and Francisco J. Ayala PART IV: POPULATION VARIATION 10. Transposons and Genome Evolution in Plants 167 Nina Fedoroff 11. Maize as a Model for the Evolution of Plant Nuclear Genomes 187 Brandon S. Gaut, Maud Le Thierry d’Ennequin, Andrew S. Peek, and Mark C. Sawkins 12. Flower Color Variation: A Model for the Experimental Study of Evolution 211 Michael T. Clegg and Mary L. Durbin 13. Gene Genealogies and Population Variation in Plants 235 Barbara A. Schaal and Kenneth M. Olsen PART V: TRENDS AND PATTERNS IN PLANT EVOLUTION 14. Toward a New Synthesis: Major Evolutionary Trends in the Angiosperm Fossil Record 255 David Dilcher

Contents / xi 15. Reproductive Systems and Evolution in Vascular Plants 271 Kent E. Holsinger 16. Hybridization as a Stimulus for the Evolution of Invasiveness in Plants? 289 Norman C. Ellstrand and Kristina A. Schierenbeck 17. The Role of Genetic and Genomic Attributes in the Success of Polyploids 310 Pamela S. Soltis and Douglas E. Soltis Index 331

Next: Part I EARLY EVOLUTION AND THE ORIGIN OF CELLS »
Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins Get This Book
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"The present book is intended as a progress report on [the] synthetic approach to evolution as it applies to the plant kingdom." With this simple statement, G. Ledyard Stebbins formulated the objectives of Variation and Evolution in Plants, published in 1950, setting forth for plants what became known as the "synthetic theory of evolution" or "the modern synthesis." The pervading conceit of the book was the molding of Darwin's evolution by natural selection within the framework of rapidly advancing genetic knowledge.

At the time, Variation and Evolution in Plants significantly extended the scope of the science of plants. Plants, with their unique genetic, physiological, and evolutionary features, had all but been left completely out of the synthesis until that point. Fifty years later, the National Academy of Sciences convened a colloquium to update the advances made by Stebbins.

This collection of 17 papers marks the 50th anniversary of the publication of Stebbins' classic. Organized into five sections, the book covers: early evolution and the origin of cells, virus and bacterial models, protoctist models, population variation, and trends and patterns in plant evolution.

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