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456 Pages·1991·15.13 MB·English
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AMPHIBIAN CYTOGENETICS AND EVOLUTION EDITED BY David M- Green Redpath Museum McGill University Montreal, Quebec, Canada Stanley K- Sessions Department of Biology Hartwick College Oneonta, New York ACADEMIC PRESS, INC. Harcourt Brace Jovanovich, Publishers San Diego New York Boston London Sydney Tokyo Toronto Front cover illustrations by Michael De Braga. Photomicrograph of chromosomes from the frog Leiopelma hochstetteri, by David M. Green. This book is printed on acid-free paper. 0 Copyright © 1991 by ACADEMIC PRESS, INC. All Rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher. Academic Press, Inc. San Diego, California 92101 United Kingdom Edition published by Academic Press Limited 24-28 Oval Road, London NW1 7DX Library of Congress Cataloging-in-Publication Data Amphibian cytogenetics and evolution / edited by David M. Green and Stanley K. Sessions. p. cm. Includes index. ISBN 0-12-297880-3 1. Amphibians-Cytogenetics. 2. Amphibians-Evolution. I. Green, David Martin. II. Sessions, Stanley Keith. QL668.5.A56 1991 597.6O415--dc20 91-2752 CIP PRINTED IN THE UNITED STATES OF AMERICA 91 92 93 94 9 8 7 6 5 4 3 2 1 Contributors Numbers in parentheses indicate the pages on which the author's contributions begin. Karen Anderson (299), Department of Biology, Hofstra University, Hempstead, New York 11550 James P. Bogart (233), Department of Zoology, University of Guelph, Guelph, Ontario NIG 2W1, Canada Harold G. Callan (217), Gatty Marine Laboratory, University of St. Andrews, Fife KY16 8LB, Scotland Jose Roberto Alegria Coto (157), Departamento de Biologia, Facultad de Ciencias y Humanidades, Universidad de El Salvador, San Salvador, El Salvador J.T. Epplen (393), Max Planck Institute for Psychiatry, Martinsried, Germany David M. Green (1, 333,431), Redpath Museum, McGill University, Montreal, Quebec H3A 2K6, Canada T. Haaf (393), Department of Human Genetics, University of Würzburg, Koellikerstr. 2, D-8700 Würzburg, Germany David M. Hillis (7), Department of Zoology, University of Texas, Austin, Texas 78712 Chikako Ikebe (67), Department of Biology, Toho University, Funabashi, Chiba 274, Japan K. Kausch (393), Department of Human Genetics, University of Würzburg, Koellikerstr. 2, D-8700 Würzburg, Germany James Kezer (89), Department of Biology, University of Oregon, Eugene, Oregon 97403 xi xii Contributors Max King (359), Museum of Arts and Sciences of the Northern Territory, Darwin, Northern Territory 0801, Australia Sei-ichi Kohno (67), Department of Biology, Toho University, Funabashi, Chiba 274, Japan Masaki Kuro-o (67), Department of Biology, Toho University, Funabashi, Chiba 274, Japan Pedro E. Leon (157), Centro de Investigaciones en Biologia Celular y Molecular (CIBCM) and Escuela de Medicina, Universidad de Costa Rica, Ciudad Universitaria Rodrigo Facio, San Jose, Costa Rica Herbert C. Macgregor (175), Department of Zoology, University of Leicester, Leicester LEI 7RH, England Giorgio Mancino (197), Dipartimento di Fisiologia e Biochimica, Laboratori di Biologia Cellulare e dello Sviluppo, via G. Carducci, 13, La Fontina, 1-56010 Ghezzano, Pisa, Italy I. Nanda (393), Department of Human Genetics, University of Würzburg, Koellikerstr. 2, D-8700 Würzburg, Germany Irma Nardi (131), Dipartimento di Fisiologia e Biochimica, Laboratori di Biologia Cellulare e dello Sviluppo, via G. Carducci 13, La Fontina, 1-56010 Ghezzano, Hsa, Italy Ronald A. Nussbaum (33), Museum of Zoology and Department of Biology, University of Michigan, Ann Arbor, Michigan 48109 M. Schmid (393), Department of Human Genetics, University of Würzburg, Koellikerstr. 2, D-8700 Würzburg, Germany Stanley K. Sessions (1, 89,431), Department of Biology, Hartwick College, Oneonta, New York 13820 C. Steinlein (393), Department of Human Genetics, University of Würzburg, Koellikerstr. 2, D-8700 Würzburg, Germany Janina Tymowska (259), Station de Zoologie Exporimentale, Universite de Gendve, 154 route de Malagnou, CH-1224, Chene-Bougeries/Geneva, Switzerland Preface Cytogenetics, the study of chromosomes, is undergoing a modern-day renaissance. Employing methods pioneered in molecular biology, molecu- lar cytogenetics promises to overcome previous limitations of classical chromosome study based on stained chromosomes. Comparative, evolu- tionary cytogenetics is reaping the benefit. This book, "Amphibian Cy- togenetics and Evolution," appears at a time when molecular cytogenetics is poised to make significant impact on evolutionary studies, enabling problems of chromosomal structure and change to be critically addressed. The early stages of any field are full of excitement; for a time, any new discovery is momentous. This is as true, for instance, of the early years of scanning electron microscopy in the 1960s and isozyme electrophoresis in the 1970s as for molecular biology in the 1980s. The early years of modern cytogenetics in the 1950s were similarly full of excitement as "squash and splash" methods for making preparations were discovered and chromo- somes could be seen in their glory. Chromosome-banding methods held even more promise of ever more precise characterization of chromo- somes. However, as in many fields that promise answers for unsolved ques- tions, the early flush of enthusiasm for a new enterprise fades as the limitations of techniques inevitably become apparent and newer methods appear. So it was for the early promise of cytogenetics for evolutionary biology, as for isozymes and, even now, for restriction fragment-length polymorphisms in molecular studies. All of these methods still have their uses, but their glamor as routes to knowledge has dimmed. Yet cy- togenetics, the direct examination of genome structure, is complementary to the examination of genome organization at the molecular level and, thus, has been rejuvenated by new methods, including use of monoclonal antibodies, DNA sequencing, and in situ hybridization, the use of which are illustrated by many of the contributions in this book. xiii xlv Preface Yet, as much as it is about cytogenetics, this book is also about amphibians. Chromosome evolution in amphibians has been far from static. Among anurans, there is great variation in chromosome number, from In = 14 in the African frog genus Arthroleptis, to In = 62 in the Chinese frog Rana phrynoides, and 8n = 104 in the South American polyploid frog Ceratophrys ornata. Within the huge frog genus Eleuthero- dactylus, with over 450 species, diploid chromosome numbers range from 18 to 36. In salamanders, diploid chromosomes number range from 22 in North American salamandrids to 78 in the hynobiid Onychodactylus ja- ponicus. Nor is polyploidy unusual in amphibians. Naturally occurring triploid, tetraploid, and even pentaploid salamanders are known in the Ambystoma jeffersonianum complex, and triploids are common in the self-perpetuating hybrid frogs known as "Rana esculenta." The North American grey treefrogs Hyla chrysoscelis and Hyla versicolor are sibling species, diploid and tetraploid, respectively, and polyploidy has character- ized the speciation of frogs in the genus Xenopus. All species in the salamander family Sirenidae appear to be polyploid, with variable chromo- some numbers and morphologies. Supernumerary chromosomes are found in many species of both salamanders and frogs. Banding studies reveal extensive diversity in the amounts, kinds, and distributions of heterochromatin, nucleolus organizer regions, and other chromosome structures. Amphibians exhibit all stages of sex chromosome differentia- tion, from complete homomorphism to extreme heteromorphism. This is readily seen within the single salamander genus Necturus and especially within the bolitoglossine plethodontid salamanders. Both male (XY/XX) and female (ZZ/ZW) heterogametic systems are present among am- phibians. Genome sizes also vary enormously, from the small 5 pg of DNA in the diploid nucleus of a Xenopus laevis to more than 165 pg of DNA in a diploid nucleus of the salamander Necturus maculosus. Even within the single family Plethodontidae, genome sizes range from 26 to > 152 pg per diploid nucleus. Phenomena such as these are critically discussed by contributors to this book. Amphibians have great advantages as subjects for chromosome study. With few exceptions, they do not have high chromosome numbers. Their chromosomes are relatively large and easy to prepare. Lampbrush chro- mosomes visible in meiotic oocyte nuclei of amphibians are ideal subjects for in situ labeling and analysis of chromosome structure. Many amphibian species, especially newts of the genus Triturus and frogs of the genus Xenopus, are easily maintained in captivity and, thus, have been widely used in genetic studies of many sorts. It is particularly valuable at this time to bring together, in a single volume such as this, the latest information about the evolutionary cytogenetics of these animals. The utility and fascination of studying amphibian cytogenetics is well Preface XV known among its practitioners, yet for those in other fields studying differ- ent groups of organisms, amphibians still have a reputation as extreme karyotypic conservatives. In talking to colleagues at the annual meeting of the American Society of Ichthyologists and Herpetologists (ASIH) in 1987, we thought that a symposium on the current state of affairs of amphibian cytogenetics would be particularly timely, especially since Jim Kezer, the teacher, colleague, and friend of amphibian cytogeneticists everywhere, was approaching his eightieth birthday. The symposium in honor of Jim Kezer, who was in attendance, was entitled "Amphibian Cytogenetics and Evolution" and hosted by the ASIH. It was organized by the editors of this book with support from the Bowerman Foundation of Oregon and held in San Francisco in 1989. Although inspired by the 1989 symposium, this book is not a sym- posium volume. Several chapters are not based on presentations given at the symposium, and some symposium papers are not included here. Gath- ered together for the first time are chapters concerning the cytogenetics of all three orders in the class Amphibia: caecilians (Gymnophiona), sala- manders (Caudata), and frogs (Anura). Each chapter deals with a specific topic of present interest. Some chapters deal primarily with chromosomal variation within particular groups, caecilians or bolitoglossine salaman- ders for example, whereas others examine more general cytogenetic phe- nomena, such as heterochromatin evolution, supernumerary chromo- somes, or sex chromosomes, across all groups of Amphibia. The result is an up-to-date and comphrehensive survey of the cytogenetics of a major class of animals with contributions by the leaders in the field around the world. "Amphibian Cytogenetics and Evolution" will be of interest to classical and molecular cytogeneticists, evolutionary biologists, herpetol- ogists, and anyone using amphibians in genetic research. All the contributions in this book were reviewed by third parties. We are grateful to J. J. Bull, C. J. Cole, J. G. Gall, D. A. Good, B. Hamkalo, R. F. Inger, R. N. Jones, A. Larson, L. R. Maxson, C. Moritz, M. Romano, R. D. Sage, S. W. Sherwood, D. B. Wake, and M. Wake for their time and helpful comments. We also thank our editor at Academic Press, Phyllis B. Moses, for her efforts on behalf of this project. Many of the tasks associated with the preparation of the manuscripts for publication were assisted by Delise Alison, Jeanne Armstrong, Hinrich Kaiser, David A. Good, Christele de Souich, and Tim Sharbel. We also thank the American Association of Ichthyologists and Herpetologists for their sponsorship of the 1989 symposium and Jay Bowerman and the Bowerman Foundation for much needed financial help in bringing the participants together. Fi- nally, we thank Jim Kezer, who continues to inspire us all. David M. Green and Stanley K. Sessions CHAPTER 1 James Kezer: A Pioneer in Amphibian Cytogenetics Stanley K* Sessions David M* Green Department of Biology Redpath Museum Hartwick College McGill University Oneonta, New York Montreal, Quebec, Canada This book is dedicated to Dr. James Kezer, Professor Emeritus at the University of Oregon in Eugene, Oregon. Jim (Fig .1) is known by friends and colleagues throughout the world not only as a pioneer in the field of amphibian cytogenetics but also because of the positive influence he has on everyone he encounters. It is impossible for anyone who has met him to forget him. The first encounter that one of us (SKS) had with Jim was in Edward Novitski's evolution course at the University of Oregon, where Jim gave a guest lecture one day on the chromosomes and evolution of plethodontid salamanders. Sessions was an undergraduate at the time and he had never before (or since) witnessed a teacher so excited about any subject. The experience had a heavy impact and in fact has influenced the course of Sessions' professional career. Jim's research interest in salamander cytogenetics has its roots in the 1930s, when Jim was working as a high school teacher in New Jersey. During the summer of 1932, he attended Cornell University where he took courses from E. L. Palmer in science education, A. A. Allen in ornithol- ogy, and A. H. Wright in herpetology and natural history. It was during this first summer at Cornell, in Wright's natural history course, that Jim had his first encounter with plethodontid salamanders. During a field trip into Cascadilla Gorge along the edge of the Cornell Campus, Wright showed to his students specimens of the common redback salamander, Plethodon einereus. This experience so inspired Jim that he incorporated natural history and herpetology into his high school science courses, including field trips where he and his students carried out systematic surveys of local vertebrates, including especially the salamanders. To pursue his interests in salamanders at deeper levels, Jim entered a Ph.D. program at Cornell in 1938, where a cytology course alerted him to the possibility of using chromosome variation to study evolutionary rela- tionships among plethodontid salamanders. A survey of the literature AMPHIBIAN CYTOGENETICS AND EVOLUTION 1 Copyrisht © 1991 by Academic Press, Inc. All Rights of Reproduction in any Form Reserved. 2 Stanley K. Sessions and David M. Green Figure 1. James Kezer in 1967 at the University of Oregon. showed that almost nothing was known about this topic at the time and so he made it the subject of his Ph.D. research. Jim's graduate work was interrupted in 1942 by World War II and a 4-year stint in the army, during which time he advanced from buck private to second lieutenant and was put in charge of bacteriology and serology for the 55th General Hospital in England and France. After leaving the army in 1946 with the rank of captain, Jim returned to graduate school at Cornell to continue his research on salamander cytogenetics. Jim's thesis work was initially extremely difficult and frustrating. The standard cytogenetic techniques of the time involved analysis of paraffin sections, which made it almost impossible to determine chromosome num- bers and morphology with any accuracy. A major breakthrough occurred when Jim began to apply squashing techniques to his salamander material (Fig. 2). Although this method had been commonly used by plant cy- togeneticists, this was the first time that it had been used for animal cells. 1. James Kezer 3 The technique produced exquisite, well-spread chromosome preparations in which chromosome number and morphology were clearly visible. Jim used this method long before human cytogeneticists began using similar methods to accurately determine the number of chromosomes in a human karyotype. With this technical success, Jim immediately launched a com- parative study of the karyotypes of all plethodontid salamanders. In one of life's strange ironies, after years of frustration and finally a breakthrough providing an effective method to examine chromosome vari- ation in detail, Jim's first major discovery was that all the plethodontid species he examined had nearly identical karyotypes with 14 bi-armed chromosomes! This discovery had two effects on his research. First, Jim decided to look for chromosomal variation at higher levels of resolution and began detailed studies of the meiotic behavior of salamander chromo- somes, whose large size (Fig. 3) turned out to be an advantage for visualiz- ing the various meiotic stages. Second, Jim decided to learn how to pre- pare and investigate the lampbrush chromosomes found in amphibian oocytes. This led to visits to H. G. (Mick) Callan's laboratory in St. Andrews, Scotland, where Jim established working relationships with Joe Figure 2. How to make a "chromosome squash" preparation.

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