The Evolutionary Biology of Hearing

871 Pages·1992·30.457 MB·English

by  Carl Gans (auth.), Douglas B. Webster, Arthur N. Popper, Richard R. Fay (eds.)

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
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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 o o
o
o
Q 3 5 7 a 9
10
1
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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 131
BERND U. BUDELMANN
Chapter 10 Hearing of Nonarthropod Invertebrates. . . . . . . . . . . . . . . . . .. 141
BERND U. BUDELMANN
Contributed Abstracts
A. The Mechanoreceptive Origin of Insect Tympanal Organs:
A Comparative Study of Homologous Nerves
in Tympanate and Atympanate Moths. . . . . . . . . . . . . . .. 156
JAYNE E. YACK AND JAMES H. fuLLARD
B. Organization of the Auditory Pathway in Noctuoid Moths:
Homologous Auditory Evolution in Insects. . . . . . . . . . .. 157
G.S. BOYAN, JAMES H. fuLLARD, AND IL.D. WILliAMS
C. Hearing in the Primitive Ensiferan Cyphoderris
monstrosa (Orthoperta: Haglidae) . . . . . . . . . . . . . . . . . .. 158
ANDREW C. MASON AND KLAUS SCHILDBERGER
D. Hair Cell Sensitivity in Cephalopod Statocyst 159
RoDDY WILliAMSON
SECTION TIl ASPECTS OF HEARING AMONG VERTEBRATES
Chapter 11 Convergence of Design in Vertebrate Acoustic Sensors 163
EDWIN R. LEWIS
Chapter 12 The Efferent Innervation of the Ear:
Variations on an Enigma. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 185
BARRY L. ROBERTS AND GLORIA E. MEREDITH
Chapter 13 Evolution, Perception, and the Comparative Method. . . . . . .. 211
WILliAM C. STEBBINS AND MITCHELL S. SOMMERS
Chapter 14 Structure and Function in Sound Discrimination
Among Vertebrates ................................... 229
RICHARD R. FAY
Section IV Anamniotes
Chapter 15 Functional and Evolutionary Implications of Peripheral
Diversity in Lateral Line Systems ....................... 267
SHERYL COOMBS, JOHN JANSSEN, AND JOHN MONTGOMERY