Monographs on 15 Theoretical and Applied Genetics
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1 Monographs on 15 Theoretical and Applied Genetics Edited by R. Frankel (Coordinating Editor), Bet-Dagan M. Grossman, Urbana. H. F. Linskens, Nijmegen P. Maliga, Piscataway. R. Riley, London
2 Monographs on Theoretical and Applied Genetics Volume 1 Volume 2 Volume 3 Volume 4 Volume 5 Volume 6 Volume 7 Volume 8 Volume 9 Volume 10 Volume 11 Meiotic Configurations A Source of Information for Estimating Genetic Parameters By J. Sybenga (1975) Pollination Mechanisms, Reproduction and Plant Breeding By R. Frankel and E. Galun (1977) Incompatibility in Angiosperms By D. de Nettancourt (1977) Gene Interactions in Development By L. 1. Korochkin (1981) The Molecular Theory of Radiation Biology By K. H. Chadwick and H. P. Leenhouts (1981) Heterosis Reappraisal of Theory and Practice Editor: R. Frankel (1983) Induced Mutations in Plant Breedin~ By W. Gottschalk and G. Wolff (1983) Protoplast Fusion Genetic Engineering in Higher Plants By Y. Y. Gleba and K.M. Sytnik (1984) Petunia Editor: K. C. Sink (1984) Male Sterility in Higher Plants By M.L.H. Kaul (1988) 'free Breeding: Principles and Strategies By G. Namkoong, H.C. Kang, and J.S. Brouard (1988) Volume 12 The Wheat Rusts - Breeding for Resistance By D.R. Knott (1989) Volume 13 Volume 14 Volume 15 Population Dynamics and the 'Iribolium Model Genetics and Demography By R. F. Costantino and R.A. Desharnais (1991) Genetic Improvement of Tomato Editor: G. Kalloo (1991) Evolution and Function of Heterostyly Editor: S.C. H. Barrett (1992)
3 Spencer C. H. Barrett (Ed.) Evolution and Function of Heterostyly With 63 Figures Springer-Verlag Berlin Heidelberg GmbH
4 Professor SPENCER C. H. BARRETT University of Toronto Department of Botany Toronto, Ontario Canada M5S 3B2 ISBN ISBN (ebook) DOI / Library of Congress Cataloging-in-Publication Data. Evolution and function of heterostyly I Spencer C. H. Barrett; ed. p. cm. - (Monographs on theoretical and applied genetics; 15) Includes bibliographical references and index. I. Heterostylism. 2. Plan ts - Evolution. I. Series. QK659.E ' dc This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer-Verlag Berlin Heidelberg 1992 Originallypublished by Springer-Verlag Berlin HeidelbergNew Yorkin The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Reproduction of the figures: Gustav Dreher GmbH, Stuttgart 'TYPesetting: International 'Iypesetters Inc., Makati, Philippines 31/ Printed on acid-free paper
5 Preface "I do not think anything in my scientific life has given me so much satisfaction as making out the meaning of the structure of heterostyled flowers" CHARLES DARWIN (1876) 1 The subject of heterostyly has fascinated biologists since Darwin's early observations and experiments on heterostylous species conducted at Down House in Kent during the middle of the last century. Darwin's studies were summarized in his classic book The Different Forms offlowers on Plants oj the Same Species published in Despite the widespread attention that heterostyly has received as a model system for genetic and evolutionary studies, there has been no comprehensive monograph on the subject since the publication of Darwin's book. The present volume is an attempt to remedy this deficiency by providing an up-to-date review of current research on heterostylous breeding systems from an evolutionary perspective. Heterostylous plants offer excellent opportunities to investigate evolutionary patterns and processes at a variety of levels of biological organization. This is because of the relatively straightforward link between genes, development, morphology and fitness in comparison with many other reproductive adaptations. In this regard the polymorphisms provide unsurpassed opportunities for integrated evolutionary studies involving experimental field and laboratory techniques for the study of plant adaptation. The diversity of approaches used to study heterostyly are reflected in the topics covered in this volume written by leading authorities in the field of plant reproductive biology. Chapters on the early history, structure, development, genetics, evolution, adaptive significance and population biology of heterostylous plants are represented. In addition, the importance of pollen-pistil interactions, gametophytic competition and the optimal allocation of resources to female and male sex function is also covered along with a review of the ways that heterostyly has been evolutionarily modified into other breeding systems. Some chapters synthesize a large and often scattered literature; others provide new theoretical insights and experimental data not previously published. This project would not have got off the ground if it were not for the enthusiasm of Marc Nicholls. On behalf of the authors I thank him for his early interest and initiative. Finally, I thank the authors for their patience and assistance in preparing this volume, Brenda Casper and Robert Ornduff for their generosity of spirit and Suzanne Barrett, William Cole and the staff at Springer-Verlag for their editorial help. SPENCER C.H. BARRETT 1 from Charles Darwin's autobiographical recollections; see "The Autobiography of Charles Darwin and Selected Letters" edited by F. Darwin (1958) Dover Publicat ions Inc., New York
6 Contents Chapter 1 Heterostylous Genetic Polymorphisms: Model Systems for Evolutionary Analysis S. C. H. BARRETT 1 Introduction Nature and Occurrence 3 3 Structure and Development 5 4 Genetics and Molecular Biology 7 5 Origin and Evolution 10 6 Function and Adaptive Significance 12 7 Pollen-Pistil Interactions 16 8 Maintenance and Breakdown 18 9 Conclusions 22 References 24 Chapter 2 R.ORNDUFF Historical Perspective on Heterostyly 1 Early Observations of Heterostyly 31 2 Darwin's Publications 33 3 Opposition to Darwin's Views 34 4 Early Field Stud ies 34 5 Early Genetic Work 36 6 Conclusions 37 References 37 Chapter 3 Floral Polymorphisms and Their Functional Significance in the Heterostylous Syndrome R. DULBERGER 1 Introduction Polymorphisms Style and Stamen Lengths Pollen Stigmas ' Functional Significance of the Polymorphisms 54
7 VIII Contents 3.1 Pollen Flow and Pollen Grain Size and Production Heteromorphic Incompatibility 57 4 Constraints Limiting the Distribution of Heterostyly 71 5 Atypical Heterostyly 72 6 Reciprocal Herkogamy, Heteromorphic Incompatibility, and Evolution of Heterostyly Hypothesis and Evidence Evolution of Heterostyly 76 References 77 Chapter 4 The Development of Heterostyly J. H. RICHARDS and S. C. H. BARRETT 1 Introduction Structure of Mature Heterostylous Flowers Constraints on Morphology of Heterostylous Flowers Structural Basis for Style and Stamen Heteromorphisms Ancillary Characters of Heterostylous Flowers Floral Development in Heterostylous Species Mature Flower Structure in Tristylous Lythrum, Oxalis, and the Pontederiaceae Development of Tristyly in Pontederiaceae Development of Tristyly in Lythraceae and Oxalidaceae Comparison of Development Among Tristylous Species Development ofdistyly Phenotypic Variation in Floral Heteromorphisms General Considerations....' Floral Variation in Eichhornia paniculata Genes and the Development of Heterostyly Development and the Evolution of Heterostyly Future Research 123 References 124 Chapter 5 The Genetics of Heterostyly D. LEWIS and D. A. JONES 1 Introduction Defin ition of Terms Evidence of the Genetic Factors S, sand M, m Linkage of Sand M Factors at the Chromosomal Level Heterostylic Characters Comparison Between Species Possible Developmental Connections Homomorphic Variants 140
8 Contents IX 6.1 Homomorphic Variants Within Species Comparisons Between Species No Heteromorphic Chromosomes Hypothesis of the Supergene 146 References 148 Chapter 6 The Evolution of Heterostyly D. G. LLOYD and C. 1. WEBB 1 Introduction Floral Characters of Families in Which Heterostyly Has Evolved The Flowers of Families with Heterostylous Species Families with Exceptional Character States Conclusion Postulates About Evolutionary Events Ancestors of Heterostylous Species Had Approach Herkogamy Reciprocal Herkogamy Preceded Self-Incompatibility and the Ancillary Features The Initial Step in the Evolution of Heterostyly is a Stigma-Height Polymorphism Diallelic Self-Incompatibility is Qualitatively Distinct from Multiallelic Self-Incompatibility. '167 4 Discussion References 175 Chapter 7 The Selection of Heterostyly D. G. LLOYD and C. J. WEBB 1 Introduction A Reevaluation of Evidence on Darwin's Hypothesis that Heterostyly Promotes Legitimate Cross-Fertilization Examination of Pollinators Pollen Loads on Stigmas Seed Set on Self-Incompatible Homostyles Future Work Models of Selection of Distyly Selection of a Stigma-Height Polymorphism ' Subsequent Selection of an Anther-Height Polymorphism and Ancillary Features Selection of Self-Incompatibility in the Absence of Reciprocal Herkogamy Selection of Self-Incompatibility in a Population with Reciprocal Herkogamy 197
9 x Contents 3.5 The Roles of Various Selective Forces A Possible Mechanism Promoting Legitimate Cross-Pollination Discussion Historical Appendix 204 References 205 Chapter 8 The Application of Sex Allocation Theory to Heterostylous Plants B.B. CASPER 1 Introduction Considerations of Gender in Heterostylous Plants Genetic Models of Style Morph Frequency " " Sex Allocation Models Gender and Morph Ratio Data Control of Morph Ratios 219 References 221 Chapter 9 Pollen Competition in Heterostylous Plants: M. A. McKENNA 1 Introduction Pre-Pollination Pollen Competition Post-Pollination Pollen Competition: An Overview Post-Meiotic Gene Expression in Pollen Genetic Influences on Pollen Growth Gene Overlap in the Gametophyte and the Sporophyte Effects of Pollen Competition on Sporophytic Traits Post-Pollination Pollen Competition and Heterostyly Competition Between Intramorph and Intermorph Pollen Pollen Competition and Style Length Polymorphisms Pollen Competition and Variable Pollen Loads Conclusion References 240 Chapter 10 Evolutionary Modifications of 'Iristylous Breeding Systems S.G. WELLER 1 Introduction Lythraceae Oxalidaceae Pontederiaceae
10 Contents XI 5 Comparison of Evolutionary Modifications of Tristyly in Lythraceae, Oxalidaceae, and Pontederiaceae Conclusions References 270 Subject Index
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