The Evolutionary Biology of Hearing Douglas B. Webster Richard R. Fay Arthur N. Popper Editors The Evolutionary Biology of Hearing With 355 Illustrations, 2 in Full Color Springer-Verlag New York Berlin Heidelberg London Paris Tokyo Hong Kong Barcelona Budapest Douglas B. Webster Richard R. Fay Department of Otorhinolaryngology Parm1y Hearing Institute Louisiana State University Medical Center and New Orleans, LA 70112, USA Loyola University of Chicago Chicago, IL 60626, USA Arthur N. Popper Department of Zoology University of Maryland College Park, MD 20742, USA Cover Illustration: WIlliam N. Tavolga Library of Congress Cataloging-in-Publication Data The evolutionary biology of hearing 1 Douglas B. Webster, Richard R. Fay, Arthur N. Popper, editors. p. cm. Based on a conference held at the Mote Marine Laboratory in Sarasota, Fla., May 20-24, 1990. Includes bibliographical references and index. ISBN-13:978-1-4612-7668-5 1. Ear-Evolution-Congresses. 2. Hearing-Congresses. 3. Physiology, Comparative-Congresses. I. Webster, Douglas B. II. Fay, Richard R. ill. Popper, Arthur N. [DNLM: 1. Ear-congresses. 2. Evolution-congresses. 3. Hearing­ congresses. 4. Histology, Comparative-congresses. 5. Invertebrates-congresses 6. Physiology, Comparative­ congresses. 7. Vertebrates-congresses. WV 270 E92 1990] QP460.EP96 1992 591.1 '825 - dc20 DNLM/DLC for Library of Congress 91-4805 CIP Printed on acid-free paper. © 1992 Springer-Verlag New York Inc. Softcover reprint of the hardcover 1st edition 1992 All rights reserved. This work may not be translated or copied in whole or in part without the written per­ mission of the publisher (Springer-Verlag New York, Inc., 175 Fifth Avenue, New York, NY 10010, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use of general descriptive names, trade names, trademarks, etc., in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. Production managed by Terry Kornak; manufacturing supervised by Rhea Talbert. Typeset by Publishers Service of Montana Inc., Bozeman, MT. 9 8 7 6 5 4 3 2 1 ISBN-13:978-1-4612-7668-5 e-ISBN-13: 978-1-4612-2784-7 DOl: 10.1007/978-1-4612-2784-7 This volume is dedicated to the memory of Professor Ernest Glen Wever (1902-1991), a pioneer in auditory research during much of the 20th century, and one of the few people who kept the flame of evolotionary biology alive in the hearing sciences. Without doubt, his ideas and work have had a major influence on all the chapters in this volume. o Q o Q 0 3 5 o 7 o a 9 o o 10 1 Q Key to Photograph of Meeting Attendees 1. W. Tavo1ga 18. M. Miller 35. T. Lewis 52. W. Stebbins 2. A. Popper 19. K. Brandle 36. N. Schell art 53. E. Allin 3. D. Webster 20. A. Mason 37. A. Musicant 54. 1. Rosowski 4. R. Fay 2l. S. Yack 38. C. Gans 55. 1. Fullard 5. R. Northcutt 22. L. Gunn 39. T. Hetherington 56. P. Narins 6. C. Platt 23. Z. Wollberg 40. E. Lombard 57. A. Michelsen 7. R. Hoy 24.1. Clack 4l. H. Romer 58. B. Budelmann 8. N. Fuzessery 25. K. Mahadevan 42. B. Lewis 59. R. Williamson 9.1. Hall 26. W. Yost 43. R. Heffner 60. 1. Montgomery lO. R. Masterton 27. 1. Hopson 44. G. Meredith 6l. B. L. Roberts 11. M. Lenhardt 28. C. Schreiner 45. W. Plassmann 62. G. Patton 12. 1. Lu 29. H. Heffner 46. M.G. Sneary 63. D. Ketten 13. 1. Crawford 30. G. Pollak 47. M. Weiderhold 64. S. Frost 14. C. Koppl 3l. 1. Christensen-Dalsgaard 48. C. McCormick 65. 1. Jannsen 15. K. Keller 32.1. Bolt 49. R. Dooling 66. P. Edds 16. C. Carr 33. E. Lewis 50. S. Coombs 67. K. Cortopassi 17. T. Bullock 34. G. Manley 51. C. von Bartheld 68. B. Fritzsch Preface To develop a science of hearing that is intellectu­ The five-day conference was held at the Mote ally satisfying we must first integrate the diverse, Marine Laboratory in Sarasota, Florida, May 20- extensive body of comparative research into an 24, 1990. The invited participants came from the evolutionary context. The need for this integra­ fields of comparative anatomy, physiology, biophys­ tion, and a conceptual framework in which it could ics, animal behavior, psychophysics, evolutionary be structured, were demonstrated in landmark biology, ontogeny, and paleontology. Before the papers by van Bergeijk in 1967 and Wever in 1974. conference, preliminary manuscripts of the invited However, not since 1965, when the American papers were distributed to all participants. This Society of Zoologists sponsored an evolutionary facilitated - even encouraged - discussions through­ conference entitled ''The Vertebrate Ear;' has there out the conference which could be called, among been a group effort to assemble and organize other things, "lively." The preview of papers, along our current knowledge on the evolutionary-as with the free exchange of information and opinion, opposed to comparative-biology of hearing. also helped improve the quality and consistency of In the quarter century since that conference the final manuscripts included in this volume. there have been major changes in evolutionary In addition to the invited papers, several studies concepts (e.g., punctuated equilibrium), in sys­ were presented as posters during evening sessions. tematics (e.g., cladistics), and in our understand­ The poster abstracts appear at the end of each ing of hearing (e. g., hair cell mechanisms). appropriate group of papers. Moreover, the study of hearing and the ear has The final half-day of the conference was devoted matured to the point where peripheral and central to discussion, in order to allow time for topics not investigations are recognized as of equal impor­ previously heard, to attempt consensus on con­ tance and are often coordinated. troversial topics, and to suggest some fruitful With these considerations in mind, we realized avenues of future research. This final session was that the time was ripe for an international confer­ videotaped and a summary is presented in the final ence on the Evolutionary Biology of Hearing, chapter of this volume. which would have a threefold purpose: to focus on the evolutionary implications of comparative Douglas B. Webster studies; to integrate central and peripheral audi­ Richard R. Fay tory studies; and to include both vertebrates and Arthur N. Popper invertebrates. January, 1991 ix Acknowledgments We are grateful to the National Institute of Deaf­ to help us with problems. Without him, and them, ness and Other Communicative Disorders (Grant the conference could not have been as successful. NS I-R13-DCOO667), the National Science Foun­ While everyone at Mote has our thanks, a few dation (Grant BNS-8912389) and the Office of deserve special mention: Dr. Robert Heuter for Naval Research (Grant N00014-90-I1799) for pro­ extraordinary help in many facets of the organiza­ viding funds to support the conference that led to tion of the meeting; Mr. Daniel Bebak, Curator of this volume. the Mote Aquarium; lab photographer, Ms. Car­ Without doubt the conference could not have men Harris; Ms. Linda Franklin and Ms. Pamela taken place without the guidance, creativity, James, Administrative Assistants; and Mr. Paul expertise, and support of Dr. William N. Tavolga, Shrader, Business Manager. We are most grateful Senior Scientist at Mote Marine Laboratory. Dr. to Ms. Sandy Hingtgen of the Holiday Inn/Lido Tavolga has become an expert on how to make con­ Beach for doing everything possible to make our ferences work. He devoted enormous amounts of stay in Sarasota a pleasant one, and to the Sarasota time and effort to assure that every detail was taken Outboard Club for use of their facilities during part care of so that the conference attendees, including of the meeting. the editors, had no cares except scientific inter­ Finally, all the participants thank Chef Alain actions. Mons of the French Affair Delicatessen in Sarasota We are also grateful to Dr. Selvakumaran for once again turning a meeting into a sensory Mahadevan, Director of the Mote Marine Labora­ experience. By delighting our senses of taste and tory. He provided outstanding facilities and the smell at mealtimes, he made the long intervening cooperation of his staff, and was always available sessions devoted to hearing much easier. xi Contents Preface ........................................... , .. " ..... ix Acknowledgments ............................................ xi Contributors ................................................ xxxvii Ernest Glen Wever: Biography and Bibliography ................... xliii RICHARD R. FAY SECTION I EVOLUTIONARY PERSPECTIVES Chapter I An Overview of the Evolutionary Biology of Hearing 3 CARL GANS Chapter 2 Comparisons of Major and Minor Taxa Reveal Two Kinds of Differences: "Lateral" Adaptations and "Vertical" Changes in Grade .................................... 15 THEODORE H. BULLOCK Chapter 3 The Phylogeny of Octavolateralis Ontogenies: A Reaffirmation of Garstang's Phylogenetic Hypothesis 21 R. GLENN NORTHCUTT Chapter 4 Evolution of the Vertebrate Inner Ear: An Overview of Ideas . 49 ARTHUR N. PoPPER, CHRISTOPHER PLATT, AND PEGGY L. EDDS SECTION II INVERTEBRATES Chapter 5 Hearing and Sound Communication in Small Animals: Evolutionary Adaptations to the Laws of Physics. 61 AXEL MICHELSEN Chapter 6 Ecological Constraints for the Evolution of Hearing and Sound Communication in Insects .................... 79 HEINER ROMER xiii xiv Contents Chapter 7 The Processing of Auditory Signals in the CNS of Orthoptera . 95 BRIAN LEWIS Chapter 8 The Evolution of Hearing in Insects as an Adaptation to Predation from Bats ................................ 115 RONALD R. Hoy Chapter 9 Hearing in Crustacea.