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Annelid Phylogeny—Molecular Analysis with an Emphasis on Model Annelids 13 Part II Evolution and Development Christoph Bleidorn 2.1 Introduction 13 5

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Annelid Phylogeny—Molecular Analysis with an Emphasis on Model Annelids 13 Part II Evolution and Development Christoph Bleidorn 2.1 Introduction 13 5 Annelids in Modern Biology Edited by Daniel H. Shain A John Wiley & Sons, Inc., Publication Annelids in Modern Biology Annelids in Modern Biology Edited by Daniel H. Shain A John Wiley & Sons, Inc., Publication Copyright © 2009 by Wiley-Blackwell. All rights reserved. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientifi c, Technical, and Medical business with Blackwell Publishing. Published by John Wiley & Sons, Inc., Hoboken, New Jersey. Published simultaneously in Canada. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) 750-8400, fax (978) 750-4470, or on the web at www.copyright.com. Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) 748-6011, fax (201) 748-6008, or online at http://www.wiley.com/go/permission. Limit of Liability/Disclaimer of Warranty: While the publisher and author have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifi cally disclaim any implied warranties of merchantability or fi tness for a particular purpose. No warranty may be created or extended by sales representatives or written sales materials. The advice and strategies contained herein may not be suitable for your situation. You should consult with a professional where appropriate. Neither the publisher nor author shall be liable for any loss of profi t or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. For general information on our other products and services or for technical support, please contact our Customer Care Department within the United States at (800) 762-2974, outside the United States at (317) 572-3993 or fax (317) 572-4002. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic formats. For information about Wiley products, visit our web site at www.wiley.com. Library of Congress Cataloging-in-Publication Data: Annelids in modern biology / edited by Daniel H. Shain. p. cm. Includes index. ISBN 978-0-470-34421-7 (cloth) 1. Annelida. I. Shain, Daniel H. QL391.A6.A56 2009 592′.6–dc22 2008042925 Printed in the United States of America. 10 9 8 7 6 5 4 3 2 1 In Memoriam Charlie D. Drewes (1946 – 2005) On Monday, July 4, 2005, those of us interested in annelids and their use as models in research and teaching lost a good friend and enthusiastic colleague. Charlie Drewes, Professor of Ecology, Evolution and Organismal Biology at Iowa State University, died in Ames, Iowa. Charlie was born and raised in Minnesota and received a bachelor ’ s degree in biology from Augustana College in South Dakota. As a National Science Foundation Fellow in the early 1970s, he completed both master ’ s and doctoral degrees in zoology at Michigan State University. He was recruited as an assistant professor to Iowa State University where he attained the rank of professor and, in 2003, was honored with the title of University Professor. As a physiologist at Iowa State University for 31 years, Charlie taught hundreds of students in neurobiology, invertebrate biology, advance vertebrate physiology and science ethics. Charlie mentored 19 graduate students in neurobiology research, many of them now mentoring students of their own at universities in California, Illinois, Texas, Vermont and Georgia, among others. He published over 50 refereed research articles and numerous book chapters, invited reviews and education - related publications. Many of his most important contributions followed his development of noninvasive, recording devices for detecting giant fi ber action potentials in freely moving worms. He applied this approach v vi In Memoriam to studies of escape refl ex physiology, annelid nerve regeneration and the sublethal effects of environmental toxicants. In the last decade or more, Charlie invested considerable effort in developing Lumbriculus variegatus as a tool for biological science education (see Chapter 10 ). With groups now interested in sequencing the genome of L. variegatus and with its expansion as a model in teaching and research laboratories, Charlie ’ s legacy might be linked to his keen enthusiasm for the California mudworm as a model for discovery. Charlie Drewes focused the last years of his life on educational outreach to high school and college science teachers. He conducted an annual “ total immersion ” teaching work- shop at Iowa Lakeside Laboratory in Lake Okoboji, Iowa. A legion of high school and community college biology teachers from 16 states participated in these workshops over the years. He conducted numerous invited workshops and presentations at local and national platforms, including a guest instructorship at the Woodrow Wilson National Fel- lowship Foundation and recurring visiting instructorships at Advanced Placement Biology workshops for State of Texas biology teachers at Texas A & M University. Thus, Charlie ’ s impact on biologists, and especially the group of individuals he fondly called wormolo- gists, was far broader than the borders of Iowa. Charlie was a recipient of several distin- guished teaching awards from Iowa State University, the Iowa Academy of Science and the National Association of Biology Teachers (NABT). In 2004, the NABT named him the National College Biology Teacher of the Year. Along with his research publications, Charlie produced a long list of useful documents, informational and procedural, on anne- lids and other invertebrates as tools for science education. This can be found online at a site ( http://www.eeob.iastate.edu/faculty/DrewesC/htdocs/ ) maintained by the Department of Ecology, Evolution, and Organismal Biology , Iowa State University. Charlie Drewes was willing to answer e - mails from wondering high school students at almost any time of the day or night. He would talk for hours at a time in person or by phone with colleagues seeking his knowledge. We will miss Charlie ’ s inexhaustible excite- ment toward biology and annelids in particular. His passing has created a void in our sci- entifi c community and in many of our hearts. Charlie enjoyed life and the lives of worms. Let us continue the joy. Contents Preface xi 3.2 Sources and Kinds of Variation 32 Contributors xiii 3.3 Examples of Clitellate Model Organisms 34 3.4 Cryptic Speciation 41 Part I Annelids as Model Systems 3.5 Conclusions and in Biology Recommendations 41 4. Annelid Life Cycle Cultures 47 1. Developing Models for Lophotrochozoan and Annelid Donald J. Reish and Bruno Pernet Biology 3 4.1 Introduction 47 Kenneth M. Halanych and 4.2 Criteria for the Selection of Elizabeth Borda Species 48 4.3 Summary of Culture 1.1 Introduction 3 Techniques 48 1.2 Phylogenetic Considerations 4 4.4 Life Cycle Cultures of 1.3 Genetic and Developmental Polychaeta 50 Tools 5 4.5 Life Cycle Cultures of 1.4 Annelid Model Organisms 6 Oligochaeta 56 1.5 Other Potential Annelid 4.6 Life Cycle Cultures of Hirudinea Models 8 (Leeches) 58 2. Annelid Phylogeny—Molecular Analysis with an Emphasis on Model Annelids 13 Part II Evolution and Development Christoph Bleidorn 2.1 Introduction 13 5. Annelids in Evolutionary 2.2 Genes 14 Developmental Biology 65 2.3 Molecular Annelid Dian-Han Kuo Phylogeny 16 2.4 Choosing Model Organisms 24 5.1 Introduction 65 2.5 Branch Lengths 24 5.2 Evo-Devo Today 66 2.6 Problems in Inferring Annelid 5.3 Evo-Devo as Comparative Phylogeny 24 Biology 66 2.7 Conclusions 25 5.4 Why Annelid Development Is Interesting for Metazoan 3. Cryptic Speciation in Clitellate Evo-Devo Biologists 67 Model Organisms 31 5.5 Case Study 1: Segmentation 68 Christer Erséus and Daniel Gustafsson 5.6 Case Study 2: Spiral Cleavage and 3.1 Introduction 31 Axis Specifi cation 74 vii viii Contents 5.7 Tools for Analyzing Molecular Part III Neurobiology and Regeneration Mechanisms of Development 79 5.8 The Future of the Annelid 8. Cellular and Behavioral Model Systems for Properties of Learning in Leech Evo-Devo 81 and Other Annelids 135 Kevin M. Crisp and Brian D. Burrell 6. Evolution, Development and 8.1 Introduction 135 Ecology of Capitella sp. I: 8.2 Learning in the Leech Whole- A Waxing Model for Polychaete Body Shortening Refl ex and Role Studies 88 of the S Interneuron 137 Susan D. Hill and Robert M. Savage 8.3 Role of the S Interneuron: Modulation of Excitability 139 6.1 Introduction 88 8.4 Learning in the Leech Swim 6.2 Speciation Studies 89 Circuit 144 6.3 Capitella Sp. 1 8.5 Using the Leech to Study Intrinsic Morphology 91 Forms of Sensitization 146 6.4 Replacement of Lost Segments 8.6 Synaptic Plasticity in Leech and Reproductive CNS 147 Trade-Offs 92 8.7 Conclusions 150 6.5 Metatrochophores, Ciliary Bands and Musculature 93 9. Development, Regeneration and 6.6 Gene Expression during Immune Responses of the Leech the Specifi cation and Nervous System 156 Differentiation of Germ Layers 95 Michel Salzet and Eduardo Macagno 6.7 Sex among the Vermes 100 9.1 Introduction 156 6.8 Annelids and the Segmentation 9.2 Background 157 Debate 101 9.3 Recent Work on the Development 6.9 A-P Polarity—Hox and ParaHox of the Nervous System 157 Genes 106 9.4 Neuronal Regeneration and 6.10 Annelid Genomics: Draft Genome Repair 169 Sequence 108 9.5 Neuroimmune Responses 173 6.11 The Future—Where Is This 9.6 Cellular and Humoral Immune Going? 109 Mechanisms: A Leech Innate Immune Response 176 7.
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