comparative vertebrate neuroanatomy evolution and …€¦ · vertebrates—anatomy. 3. nervous...

COMPARATIVE VERTEBRATENEUROANATOMY

Evolution and AdaptationSecond Edition

ANN B. BUTLERProfessorKrasnow Institute for Advanced Study and Department of PsychologyGeorge Mason UniversityFairfax, Virginia

WILLIAM HODOSDistinguished University ProfessorDepartment of PsychologyUniversity of MarylandCollege Park, Maryland

A JOHN WILEY & SONS, INC., PUBLICATION

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COMPARATIVE VERTEBRATE NEUROANATOMY

COMPARATIVE VERTEBRATENEUROANATOMY

Evolution and AdaptationSecond Edition

ANN B. BUTLERProfessorKrasnow Institute for Advanced Study and Department of PsychologyGeorge Mason UniversityFairfax, Virginia

WILLIAM HODOSDistinguished University ProfessorDepartment of PsychologyUniversity of MarylandCollege Park, Maryland

A JOHN WILEY & SONS, INC., PUBLICATION

Copyright © 2005 by John Wiley & Sons, Inc. All rights reserved.

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Library of Congress Cataloging-in-Publication Data:Butler, Ann B.

Comparative vertebrate neuroanatomy : evolution and adaptation / Ann B. Butler,William Hodos.

p. cm.Includes bibliographical references and index.ISBN 0471210056 (alk. paper)1. Neuroanatomy. 2. Vertebrates—Anatomy. 3. Nervous system—Evolution.

4. Anatomy, Comparative. 5. Nervous system—Adaptation. I. Hodos, William.II. Title.QM451.B895 1996596¢.048—dc20 95-49380

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This dedication is in four parts: to those special friends,mentors, and family members who are now deceased, to those special persons still living who have taught and guidedus in our careers, to a special friend of the field, and to ourfamilies.

In recognition of those special persons who are nowdeceased, Ann Butler dedicates her contribution to this workto the memory of Alexander and Ethel Benedict Gutman,Raymond C.Truex, and B. Raj Bhussry;William Hodos dedicateshis contribution to the memory of his parents, Morris andDorothy Hodos, and Walle J. H. Nauta.

In recognition of those special persons in our lives whohave been teachers and mentors as well as friends and col-leagues, we also dedicate this book to Warren F. Walker, Jr.,Theodore J. Voneida, R. Glenn Northcutt, Ford F. Ebner, Sven

O. E. Ebbesson, C. Boyd Campbell, and Harvey J. Karten. Addi-tionally, we dedicate this work to Harold J. Morowitz, James L.Olds, Robert F. Smith, and William S. Hall in acknowledgementof their outstanding support and encouragement.

We also dedicate this book to Dr. Thomas Karger in appre-ciation of his generous and steadfast support of the field ofcomparative neurobiology, as particularly evinced by his sponsorship of the J. B. Johnston Club and its yearly KargerSymposium. His beneficence has substantially promoted thedissemination of new data and theories in the field and thusmaterially aided the preparation of this second edition.

Finally, we dedicate this book to our families, Thomas andWhitney Butler and Nira, Gilya, and Tamar Hodos, who havealways given us their loyal support, their patience, and theirceaseless encouragement.

Dedication

Preface xvAcknowledgments xixList of Boxes xxi

Part One

EVOLUTION AND THE ORGANIZATION OF THE CENTRAL NERVOUS SYSTEM

1 Evolution and Variation 3Introduction, 3

Diversity Over Time, 4

Evolutionary Mechanisms, 5

Genetic Factors, 5

Natural Selection, 5

Evolution of the Vertebrate Central Nervous System, 7

Sameness and Its Biological Significance, 8

Analogy, 8

Historical Homology, 8

Homoplasy, 9

Biological Homology, 11

Generative Homology or Syngeny, 12

Analysis of Variation, 13

Cladistic Analysis, 13

Parsimony, 14

Tests of Homology, 15

A Word of Caution, 15

Reconstructing Evolution, 16

2 Neurons and Sensory Receptors 19Introduction, 19

The Nervous System, 19

Neurons and Sensory Receptors, 20

Transport Within Neurons, 21

Classification of Neurons, 21

Somata, 21

Dendrites, 21

Axons, 23

Synapses, 23

Chemical Synapses, 23

Neuroactive Substances, 24

Electrical Synapses, 26

Volume Transmission, 26

Neuronal Populations, 26

Golgi Type I and II Cells, 26

Nuclei and Planes of Section, 27

Techniques for Tracing Connections Between Nuclei, 27

Receptors and Senses, 28

How Many Senses? 29

Receptors and Awareness, 29

Sensory Experience as a Private Mental Event, 30

Sensory Adaptation, 30

Receptor Types, 30

Mechanoreceptors, 31

Radiant-Energy Receptors, 34

Chemoreceptors, 37

Nervus Terminalis: An Unclassified Receptor, 41

Electroreceptors, 41

Nociceptors, 42

Magnetoreceptors, 43

Topographic Organization, 43

Receptive Fields, 46

The Senses and Evolution of the Central NervousSystem, 46

3 The Vertebrate Central Nervous System 49Introduction, 49

Development of the Brain, 49

Segmental Development of the Vertebrate Brain, 50

Neurogenesis and Migration of Neurons, 54

Cortices and Nuclei, 55

Differing Patterns of Development, 57

Ontogeny and Recapitulation, 60

Contents

vii

viii C O N T E N T S

The Brain and Spinal Cord, 61

Cellular Organization of the Central Nervous System, 61

Regional Organization of the Nervous System, 63

The Spinal Cord, 63

The Brain, 63

The Meninges and the Ventricular System, 66

Major Systems of the Brain, 67

Sensory Systems, 68

Motor Systems, 68

Nomenclature of the Brain, 69

4 Vertebrate Phylogeny and Diversity in Brain Organization 73Introduction, 73

Vertebrate Phylogeny, 74

Chordate Relationships, 74

Jawless Vertebrates, 74

Chrondrichthyes, 76

Actinopterygii, 76

Sarcopterygii, 76

The Big Picture of Vertebrate Evolution, 84

Two Types of Brain Organization, 84

Laminar Brains (Group I), 86

Elaborated Brains (Group II), 87

Glia and Brain Elaboration, 89

Laminar and Elaborated Brains across Evolution, 89

5 Evolution and Adaptation of the Brain,Behavior, and Intelligence 93Phylogeny and Adaptation, 93

Phyletic Studies, 93

Adaptation Studies, 94

The Phylogenetic Scale, 95

The Phylogenetic Tree, 95

Complexity and Evolution, 96

Anagenesis, 97

Grades of Evolutionary Advancement, 99

Evolutionary Change, 99

Brain Evolution and Behavioral Adaptation, 100

Brain Size and Brain Allometry, 100

Brain Size and Behavioral Adaptation, 105

Brain Size and Intelligence, 106

What Is Intelligence? 108

Summary and Conclusions, 109

6 Theories of Brain Evolution 113Introduction, 113

Some Common Assumptions, 113

Previous Theories of Vertebrate Brain Evolution:Addition of Structures or Areas, 114

MacLean, 114

Flechsig and Campbell, 114

Sanides, 115

Previous Theories of Vertebrate Brain Organization:New Formation and Reorganization of Circuits, 115

Herrick, 115

Bishop, 115

Ariëns Kappers, 115

Bowsher, 115

Diamond and Hall, 116

Critique of Previous Theories of Vertebrate BrainEvolution, 116

Parcellation Theory, 117

Ebbesson, 117

Deacon, 117

Current Theories of Forebrain Evolution, 117

Forebrain Evolution: Experimental Foundations, 117

Karten: Equivalent Cell Hypothesis, 118

Other Theories of Pallial Evolution, 119

Perspective, 121

Part Two

THE SPINAL CORD AND HINDBRAIN

7 Overview of Spinal Cord and Hindbrain 127Overview of the Spinal Cord, 127

Segmentation Within the Spinal Cord, 127

Roots and Ganglia, 128

Columns of the Spinal Cord, 129

Pathways Within the Spinal Cord, 130

Reflexes, 131

Spinal Autonomy, 133

Rhythmic Movements and Central Pattern Generators, 133

Overview of the Hindbrain, 133

The Obex and the Fourth Ventricle, 135

The Pontine Nuclei, 135

Ganglia of the Cranial Nerves, 135

Organization of the Cranial Nerves, 135

Embryology of the Hindbrain and a NewClassification of Cranial Nerves, 135

Efferent Axons in Afferent Nerves, 136

Evolutionary Perspectives on the Spinal Cord andHindbrain, 136

The Transition to Land, 136

Tetrapod Locomotor Patterns, 137

C O N T E N T S ix

8 The Spinal Cord 139

Muscles and Locomotion, 139

Cell and Fiber Columns, 139

Giant Axons and Escape, 141

Electromotor Neurons, 144

The Curious Spinal Cords of Sharks, 144

Ascending and Descending Pathways, 144

Reissner’s Fiber, 145

The Organization of the Tetrapod Spinal Cord, 145

Locomotor Patterns and Spinal Cord Organization, 145

The Curious Spinal Cords of Birds, 146

Segmental Organization, 147

Lamination, 147

Intrinsic Spinal Neurons, 148

Somatotopic Organization of the Ventral Horns, 148

Renshaw Cells, 149

Axon Columns and Cell Columns, 149

Marginal Cells, 150

Accessory Lobes, 150

Ascending Spinal Pathways, 150

Descending Spinal Pathways, 150

Tetrapod Central Pattern Generators, 152

Evolutionary Perspective, 152

9 Segmental Organization of the Head,Brain, and Cranial Nerves 157“Twelve” Cranial Nerves, 157

The Vertebrate Head: Segmental Organization, 158

Head Skeleton, 159

The Striated Musculature of the Head, 159

Neural Crest and Placodes, 162

Segmentation of the Head, 164

Theoretical Head Segments, 165

Segmental Organization of the Individual Cranial Nerves, 166

The Forebrain, 168

The First Head Segment, 168

The Second Head Segment, 169

The Third Head Segment, 169

The Fourth Head Segment, 169

The Fifth Head Segment, 170

10 Functional Organization of the Cranial Nerves 173Introduction, 173

The Cranial Nerves and the Spinal Cord, 173

The Organization of Sensory and Motor Columns of theCaudal Brainstem, 176

Afferent Columns of the Brainstem, 177

Efferent Columns of the Brainstem, 179

Five Cranial Nerves Rostral to the Brainstem, 180

General Considerations, 181

11 Sensory Cranial Nerves of the Brainstem 183Introduction, 183

Dorsal Cranial Nerves: Sensory Components for GeneralSomatosensory Sensation, 183

Somatosensory Innervation of the Head, 184

Central Terminations of the Trigeminal Nerve, 185

The Mesencephalic Division of the Trigeminal System, 185

Secondary Connections of the Trigeminal Nuclei, 186

Ventrolateral Placodal Cranial Nerves: Taste, 189

The Gustatory System, 190

The Gustatory Nerves and the Nucleus Solitarius, 190

Secondary Connections of the Gustatory Nucleus and Nucleus Solitarius, 190

Cyprinid and Silurid Gustatory Specializations, 192

Dorsolateral Cranial Nerves: Lateral Line and OctavalSystems, 194

The Lateral Line System, 195

The Octaval System, 196

12 Motor Cranial Nerves 205Introduction, 205

Feeding and Swallowing, 207

The Neural Control of Feeding and Swallowing, 209

The Communication Systems of Fishes, 211

The Acoustic Reflex, 213

Motor Control of Eye Muscles, 214

The Extraocular Muscles in Jawless Vertebrates, 214

The Extraocular Muscles in Jawled Vertebrates, 214

The Intraocular Muscles, 215

Central Control of the Eye Muscles, 215

The Oculomotor Complex, 217

Coordination of Eye Muscle Action, 218

Evolutionary Perspective on the Hindbrain and Midbrain Cranial Nerves, 218

13 The Reticular Formation 221Introduction, 221

The Organization of the Reticular Formation, 222

Neurons of the Reticular Formation, 222

Giant Reticulospinal Neurons, 223

Nomenclature of the Reticular Formation, 224

The Reticular Formation of the Medulla, Pons, andMidbrain, 225

The Reticular Formation of the Diencephalon, 228

Pathways of the Reticular Formation, 230

Chemical Pathways of the Reticular Formation, 232

The Spinal Cords of Nontetrapods, 139

x C O N T E N T S

The Reticular Formation and Sleep, 234

Evolutionary Perspective on the Reticular Formation, 236

14 The Cerebellum 241Introduction, 241

Overview of the Cerebellum, 241

Cerebellar Size, 242

The Various Forms of the Cerebellum, 243

Corpus Cerebelli, 243

Electroreception and the Cerebellum, 244

The Cerebellar Auricle, 245

Phyletic Development of the Form of the Cerebellum, 245

The Cerebella of Tetrapods, 246

The Cerebella of Nontetrapods, 246

Agnathans and Cartilaginous Fishes, 246

Ray-Finned Fishes, 246

The Cerebellar Cortex, 247

The Purkinje Cell Layer, 247

The Granule Cell Layer, 249

The Molecular Layer, 253

Afferent Inputs to the Cerebellar Cortex, 253

Interconnections Within the Cerebellar Cortex, 255

The Precerebellar Nuclei, 256

Cerebelloid Structures Associated With the

Fishes, 259

Cerebellar Efferents and the Deep Cerebellar Nuclei, 260


Functions of the Cerebellum, 262

Part Three

THE MIDBRAIN

15 Overview of the Midbrain 267Introduction, 267

The Isthmus, 268

The Tegmentum, 273

The Tectum, 273

16 Isthmus 275Introduction, 275

Nuclei of the Raphe, 275

Group I, 275

Group II, 275


Locus Coeruleus, 277

Group I, 277

Group II, 277


Nucleus Isthmi, 281

Group I, 281

Group II, 281


Isthmo-Optic Nucleus, 283

Group I, 283

Group II, 283


Midbrain Locomotor Region and PedunculopontineTegmental Nucleus, 284

Group I, 284

Group II, 284


Interpeduncular Nucleus, 285

Group I, 285

Group II, 285


17 Tegmentum and Tori 289Introduction, 289

Mesencephalic Nucleus of the Trigeminal Nerve, 289

Group I, 289

Group II, 290


Red Nucleus and Related Nuclei, 290

Group I, 290

Group II, 290


Substantia Nigra and Ventral Tegmental Area, 292

Group I, 293

Group II, 294


Torus Lateralis, 304

Group I, 304

Group II, 304


Torus Semicircularis, 304

Group I, 304

Group II, 305


18 Optic Tectum 311Introduction, 311

Overview of Tectal Organization, 311

Overview of Tectal Connections, 312

The Optic Tectum in Group I Vertebrates, 315

257

The Exceptional Cerebella of Weakly Electric

Cerebellum in Nontetrapods,

C O N T E N T S xi

Lampreys, 315

Squalomorph Sharks and Ratfishes, 316

Nonteleost Ray-Finned Fishes, 316

Amphibians, 319

The Optic Tectum in Group II Vertebrates, 321

Hagfishes, 321

Galeomorph Sharks, Skates, and Rays, 322

Teleosts, 322

Amniotes, 325


Part Four

THE FOREBRAIN: DIENCEPHALON

19 Overview of the Forebrain 343Introduction, 343

Nomenclature of the Forebrain in Amniotes, 344

The Diencephalon, 344

Pretectum, 344

Posterior Tuberculum, 344

Epithalamus, 345

Dorsal Thalamus, 346

Ventral Thalamus, 347

Hypothalamus and Preoptic Area, 352

The Telencephalon: Pallium, 352

The Telencephalic Pallium of Mammals, 353

The Telencephalic Pallium of NonmammalianAmniotes, 361

The Telencephalon: Subpallium, 364

The Ventrolateral Telencephalon of Anamniotes, 364

The Ventrolateral Telencephalon of Mammals, 364

The Ventrolateral Telencephalon of NonmammalianVertebrates, 368

The Septum, 369

20 Pretectum, Accessory Optic System, andMigrated Posterior Tuberculum 373Introduction, 373

Pretectum, 373

Group I, 374

Group II, 375

Accessory Optic System, 389

Group I, 391

Group II, 392


Migrated Posterior Tuberculum, 396

Group I, 396

Group II, 396


21 Epithalamus 407Introduction, 407

Epiphysis, 407

Habenula, 409


22 Dorsal Thalamus 417Introduction, 417

Collothalamic Auditory System, 418

Group I, 418

Group IIA, 418

Group IIB, 420

Collothalamic Visual and Somatosensory Systems, 426

Group I, 427

Group IIA, 430

Group IIB, 430

Lemnothalamus, 432

Group I, 432

Group IIA, 434

Group IIB, 434


Collothalamus, 437

Lemnothalamus, 437

A New Definition of the Dorsal Thalamus in Vertebrates, 439

23 The Visceral Brain: The Hypothalamus and the Autonomic Nervous System 445Introduction, 445

The Hypothalamus, 445

The Hypothalamus and the Endocrine System, 446

Circumventricular Organs, 449

Biological Rhythms, the Epiphysis, and theHypothalamus, 449

The Hypothalamus and the Limbic System, 450

The Preoptic Area, 450

The Hypothalamus in Anamniotes, 451

Jawless Fishes, 451

Cartilaginous Fishes, 451

Actinopterygians, 451

Sarcopterygians, 455

The Hypothalamus in Amniotes, 455

Connections of the Hypothalamus in Reptiles andBirds, 456

Connections of the Hypothalamus in Mammals, 457

Functions of the Hypothalamus, 460

The Autonomic Nervous System, 460

Autonomic Neurochemistry, 462

Amniotes, 462

Anamniotes, 462


xii C O N T E N T S

Part Five

THE FOREBRAIN: TELENCEPHALON

24 Basal Telencephalon 471Introduction, 471

The Striatopallidal Complexes, 472

Group I, 472

Group IIA, 476

Group IIB, 477

The Striatal Amygdala, 487

Cholinergic Neuronal Populations of the BasalTelencephalon, 488


25 Nonlimbic Pallium 495Introduction, 495

The Nonlimbic Pallium in Group I Vertebrates, 496

The Nonlimbic Pallium in Group IIA Vertebrates, 498

Neuroanatomical Organization, 498

Behavioral Issues, 501

The Nonlimbic Pallium in Amniotes, 501

Mammals: Neocortex, 501

Mammals: Claustrum-Endopiriform Formation andFrontotemporal Amygdala, 504

Reptiles and Birds, 504

Ascending Sensory Pathways to the Pallium inAmniotes, 507

Pallial Evolution and Persistent Questions of Homologies, 510

26 Visual Forebrain in Amniotes 523Introduction, 523

Ipsilateral Retinal Pathways and Stereoscopic Vision, 524

Visual Pathways to the Telencephalon in Mammals, 524

Lemnothalamic Visual Forebrain, 524

Collothalamic Visual Forebrain, 536

Pathways to the Visual Telencephalon in Reptiles andBirds, 537

Lemnothalamic Visual Pathways, 538

Collothalamic Visual Pathways, 540

Evolutionary Trends in the Visual System of Amniotes, 540

27 Somatosensory and Motor Forebrain inAmniotes 547Introduction, 547

The Somatosensory and Motor Forebrain of Mammals, 547

The Ventral Tier Nuclei of the Dorsal Thalamus, 548

Somatosensory Lemnothalamus, 548

Somatosensory Collothalamus, 548

Motor Lemnothalamus, 548

Afferents to Somatosensory Cortex, 549

Efferents of Somatosensory Cortex, 549

Pain Pathways, 549

Somatotopic Organization, 552

Motor Cortex, 557

Multiple Motor Representations of the Body, 558

The Cortical Eye Fields, 558

Afferents and Efferents of the Motor Cortex, 558

The Somatosensory and Motor Forebrain ofNonmammalian Amniotes, 559

Somatosensory System, 559

Motor System, 564


28 Auditory and Vocal Forebrain in Amniotes 571Introduction, 571

Location of Sound Sources, 571

Echolocation, 572

Auditory Channels for Time and Intensity, 573

Design Features of the Auditory System, 574

Topographic Organization, 574

Bilateral Interaction in the Auditory Pathway, 574

Descending Auditory Pathways, 574

Auditory Pathways in Tetrapods, 574

Auditory Telencephalon, 577

Columnar Organization, 577

Mammals, 577


Vocal Telencephalon, 580

Vocalization and Hearing, 581

Anurans, 582


Mammals, 587


29 Terminal Nerve and Olfactory Forebrain 593Introduction, 593

Olfactory System, 593

Group I, 594

Group II, 595

Vomeronasal System, 601

Terminal Nerve, 605


30 Limbic Telencephalon 611Introduction, 611

The Limbic Pallium in Anamniotes, 612

C O N T E N T S xiii

Group I, 612

Group IIA, 613

The Limbic Pallium in Amniotes (Group IIB), 617

Limbic Pallium of Mammals, 619

Limbic Pallium in Nonmammalian Amniotes, 623

Limbic Subpallium: Septum, 628


Part Six

CONCLUSION

31 Evolution of Brains: A Bilaterian View 637Introduction, 637

Invertebrate Brains and the Inversion Hypothesis, 638

Insect Brain Organization, 639

Urbilateria and the Ancestral Condition of Bilaterian Brains, 641

Deuterostomes and Dorsoventral Inversion, 641

Brain Evolution within Chordates, 644

The Origin of Vertebrates, 649

Haikouella, 650

Sensory System Evolution in the Vertebrate Lineage, 652

Organization of the Vertebrate Brain, 653

The Advent of Jaws, 655

Onto the Land and Into the Air, 656

Theories of Vertebrate Brain Evolution, 657

How Vertebrate Brains Evolve, 657

Appendix: Terms Used in Neuroanatomy 665Introduction, 665

Direction and Location Terms, 665

Planes of Section, 666

Neuroanatomical Names, 668

Derivation of Terms, 668

Glossary 671Index 679

What Is This Book About?This book is about the central nervous system of those

animals that possess backbones—the vertebrates—and howevolution has shaped and molded their bodies and theirnervous systems, allowing them to thrive in their particularenvironments or to take advantage of new environmentalopportunities.Thus, it is a book about the relationship betweenstructure and function and about survival through effectivedesign. It is a book about the past as well as the present andabout the history of vertebrate nervous system evolution, tothe extent that we can read that history from the present stateof these animals.

Who Is This Book For?This book has been written first and foremost for neuro-

science students at the graduate or advanced undergraduatelevel. We have presumed that the reader will have taken oneor more introductory undergraduate biology courses or other-wise be familiar with this material. In a more general sense, thisbook is also for anyone who is interested in the anatomy of thenervous system and how it is related to the way that an animalfunctions in its world, both internal and external.

This book is intended as an introductory work rather thanas a handbook or reference work that scientists might refer toin their professional writing. We have modeled this book onseveral textbooks designed for advanced undergraduate tograduate levels: Functional Anatomy of the Vertebrates: AnEvolutionary Perspective (Second Edition) by W. F. Walker, Jr.and K. F. Liem (Saunders College Publishing, Fort Worth, TX,1994); Hyman’s Comparative Vertebrate Anatomy edited byM. H. Wake (The University of Chicago Press, 1979); TheHuman Brain and Spinal Cord by L. Heimer (Springer-Verlag,New York, 1983); Core Text of Neuroanatomy by M. B.Carpenter (Williams and Wilkins, Baltimore, 1991); An Intro-duction to Molecular Neurobiology by Z. W. Hall (SinauerAssociates, Sunderland, MA, 1992); and Principles of Neuro-science (Third Edition) by E. R. Kandel, J. H. Schwartz, and T.M. Jessell (Appleton and Lange, Norwalk, CT, 1991). In keepingwith the format of these texts, we have not cited references inthe body of the text, but at the end of each chapter we havelisted the references from which we drew material and addi-tional papers that may interest the reader. Our aim has been tointroduce the reader to the field and to synthesize informationinto a coherent overview, rather than to present an extensivecatalog of individual data.

In keeping with the introductory nature of this work, welargely have omitted details on whether and/or where particu-lar projections cross the midline of the nervous system. Insome cases, where this information is of particular importance,we have included it. However, in most cases, we leave it to theinterested reader to glean such details from other sources.

This is a book that we hope will be of interest to thegeneral scientific reader and the nature enthusiast, as well asto advanced undergraduate or beginning graduate students inthe neurosciences. Physicians and others with knowledge ofthe human central nervous system should also find much ofinterest here. To our colleagues who are specialists in the fieldof comparative neuroanatomy, we say that this is not the bookthat you might write; this is the book that students should readto give them the background to read your book and otherscholarly publications in neuroanatomy and brain evolution.

Apropos of this aim and since the time of the first editionof this textbook, a truly remarkable contribution to the lit-erature of comparative neuroanatomy was made by RudolfNieuwenhuys, Hans ten Donkelaar, and Charles Nicholson withthe publication of their comprehensive and encyclopedic setof three volumes on The Central Nervous System of Verte-brates (1998, Springer-Verlag, Berlin).These volumes cover thesubject and the literature in far greater depth and breadth thancould or should be included in a textbook. We have benefitedgreatly from the material in these volumes in writing thesecond edition of this book. In updating material, there is the constant temptation to add more and more detail, and inthe process, forsake the original purpose.We thus have endeav-ored to tread a fine line between updating and maintaining theintroductory level. We hope that this book will continue to fillits intended role as an introductory work, allowing the readerto then delve into the Nieuwenhuys et al. volumes as well asthe primary literature for much more extensive and detailedtreatments of a multitude of topics.

What Can Be Learned About the HumanBrain From a Book About the Brains of ManyDifferent Vertebrates?During the past four decades, a great explosion of infor-

mation about the anatomy of the brains of nonhuman and espe-cially nonmammalian vertebrates has taken place. One of thelessons to emerge from this wealth of new data has been thereversal of the nineteenth century view that a dramatic changein brain evolution occurred with the evolution of mammals in

Preface

xv

xvi P R E FAC E

general and humans in particular. In other words, once thepowerful tools of modern neuroanatomy were applied to thebrains of birds, fishes, reptiles, and amphibians, many of the same patterns of cell groups and their interconnections thatwere known to be present in mammals (including primates)were found to be present in nonmammalian vertebrates as well.Thus, comparative neuroanatomists came to recognize that theevolution of the vertebrate central nervous system had beenfar more conservative than earlier investigators had realized.

To be sure, great differences in specialization of the brainexist between animals that have become adapted to very dif-ferent modes of existence. Indeed, those differences in formand function are what make the study of comparative neu-roanatomy and brain evolution so fascinating—a fascinationthat we hope to share with you. In spite of these differences,however, all vertebrate central nervous systems share acommon organizational scheme so that someone who is famil-iar with the brain of any vertebrate will also be on familiarground when first encountering the brain of any other species.Someone who has read this book and retained the general principles of brain anatomy and organization that it presentswill have little difficulty reading a medical school textbook ofhuman neuroanatomy because much of it will be familiar bothin overall conception and in many of the details.

What Is New in This Book and How Does ItDiffer from Other Texts?The first edition of this book incorporated several new

approaches to the subject matter of comparative neuroanatomyand the orientation with which we study it. These newapproaches, which have been maintained and/or furtherdeveloped in this second edition, include

• A recent reevaluation of the cranial nerves of vertebratesand their derivation and organization

• A new organizational approach to the various groups ofvertebrates based on the degree of elaboration in theircentral nervous systems rather than the traditional, scalanaturae-like ranking

• New insights into the organization and evolution of thedorsal thalamus and dorsal pallium in the forebrain

• A new and comprehensive overview of brain evolution invertebrates that encompasses many of the evolutionaryand developmental topics covered in the rest of the text

The first of these new approaches is based on the work ofNorthcutt, Baker, Noden, and others, on the organization of thecranial nerves. While constituting a radical departure from theestablished, traditional list of twelve cranial nerves with theirfunctional components, we feel that this new approach is amarked improvement for two reasons: First, it takes intoaccount additional cranial nerves, both long known and newlyrecognized ones, that are found in many vertebrates but are notincluded in the “traditional twelve.” Second, it is based onembryological development, including gene expression pat-terns, and thus provides a coherent accounting of the seg-mentation of the head itself and of its component parts,including both the brain and other tissues (particularly the

neural crest, epithelial placodes, and paraxial mesoderm).Chapter 9 on the embryology of the cranial nerves in relationto head segmentation covers this newly developed approachto cranial nerve organization and is crucial to understandingthe subsequent chapters on the cranial nerves themselves.

The second departure from tradition that we took in thefirst edition and have retained here is the order in whichvarious groups of vertebrates are considered in the chapters onthe various regions of the nervous system. This approach isbased on the range of variation in brain structure within eachof the major groups of vertebrates. It is intended to overcomethe erroneous but culturally ingrained idea of a single, simple-to-complex, linear series of evolutionary stages leading fromfish to frog to rat to cat to monkey to human, i.e., the myth ofa scala naturae. Chapter 4 specifically addresses this issue.

A great diversity in brain organization has been achievedindependently at least four separate times within four separateradiations of vertebrates; our approach is designed to highlightboth the diversity itself and its multiple, independent devel-opment. Thus, in a number of the chapters on brain regionsand systems, particularly in the midbrain and forebrain, we firstconsider and compare those species within each radiation inwhich the brain has relatively simple cellular organization, asfor example, lampreys, dogfish sharks, gars, and frogs. We thenconsider and compare those species within each radiation inwhich the brain has relatively complex cellular organization, asfor example, hagfishes, skates, teleost fishes, and amniotes(mammals, reptiles, and birds).We hope to convince the readerthat the development of a more complex brain has beenaccomplished not just once for the “ascent of man,” but multi-ple times. Moreover, we will show that mammals (includingprimates) do not always have the most sophisticated brainsystems.

In line with this point, other chapters, including “Evolu-tion and Variation,” “Evolution and Adaptation of the Brain,Behavior, and Intelligence,” and “Theories of Brain Evolution,”seek to dispel further the myth of scala naturae and to dealwith the actual range of variation in line with the known factsand processes involved. In this context, we hope that thereader will come to understand that, whereas some vertebrateshave simpler brains than others, all living vertebrates areequally successful in that they are alive and adapted to theirenvironments.

A third new approach taken for the first edition and main-tained here concerns the evolution of two major parts of theforebrain, the dorsal thalamus and the dorsal pallium, particu-larly in amniote vertebrates. Two fundamentally different divi-sions of the dorsal thalamus recently have been recognized inall jawed vertebrates: one that predominantly receives direct,lemniscal sensory and related inputs, called the lemnothala-mus, and one that predominantly receives sensory inputsrelayed to it via the roof of the midbrain, called the collothala-mus. These lemnothalamic and collothalamic divisions of thedorsal thalamus have recently gained validation from differen-tial patterns of gene expression during development. Corre-spondingly, two major divisions of the pallium in amniotevertebrates that receive their respective inputs predominantlyfrom the lemnothalamic and collothalamic divisions of thedorsal thalamus have been recognized as well. The way inwhich a number of the chapters on the forebrain have been

P R E FAC E xvii

organized and the material presented in them are based tosome extent on these new concepts of forebrain evolution.Finally, new insights into the evolution of the brain, not just invertebrates but among some of the invertebrate chordates aswell, are presented in the last chapter of this book. Recent find-ings on genetic patterning of central nervous system structureand on the anatomy of the brain and head region in thecephalochordate Branchiostoma, as well as anatomical evi-dence from the recently found fossils of the chordate Haik-ouella, allow for some of the features of the brain in the earliestvertebrates to be identified. A new survey of brain evolution ispresented. For context, brain organization in some inverte-brates is surveyed, particularly in terms of gene expression pat-terns, which are strikingly similar to those in vertebrates. Thenvertebrate brain evolution is discussed, beginning with a fewbut significant features that can be identified in the commonancestors of cephalochordates and vertebrates, identifying

additional features that were present in the earliest vertebrates,including two novel tissues of the head (neural crest and pla-codes) and a number of cranial nerves associated with them,and then tracing the separate evolutionary histories of the brainin the major radiations of extant vertebrates.

For the second edition, a recently proposed model of thetransition to vertebrates that specifies the gain of paired eyesand elaboration of the diencephalon and hindbrain before mostof the elaboration of neural crest and placodal tissues occurredto produce the peripheral nervous system has been included.This model was recently given strong support by newly dis-covered fossil evidence from the chordate Haikouella. Also,the striking similarities of patterning gene expression across allbilaterally symmetrical animals studied, from mice to fruit flies,and their implications for the evolution of rostrocaudally and dorsoventrally organized central nervous systems are discussed.

A number of our colleagues have read portions of the firstand/or second editions for us or have discussed a variety of thetopics with us.They also sustained us with their enthusiasm forthis project. We owe a large debt of gratitude to Philip Zeigler,who served as editor of the first edition and provided us withdetailed and thoughtful commentary on all of the chapters.Thebook was greatly improved as a result of his efforts. We thankAndrew Bass, Steven Brauth, Catherine Carr,William Cruce, thelate William Dingwall, Joseph Fetcho, Michael Fine, KatherineFite, Jon Kaas, Harvey Karten, Darcy Kelley, Wayne Kuenzel,Harry Jerison,Thurston Lacalli, Michael Lannoo, Rodolfo Llinás,Paul Manger, Gloria Meredith, Donald Newman, RudolfNieuwenhuys, Glenn Northcutt, Mary Ann Ottinger, MichaelPritz, Luis Puelles, Anton Reiner, Daphne Soares, Charles Sternheim, Mario Wullimann, David Yager, and several anony-mous reviewers for their comments and suggestions on various chapters for the first and/or second edition. We aregrateful to them for their advice and suggestions and for inter-cepting various errors. We accept full responsibility for anyerrors that remain despite our best efforts. We also thank WallyWelker for providing several photomicrographs of raccoonbrain sections. We owe a special debt of gratitude to R. GlennNorthcutt for providing original negatives of Nissl-stained sec-tions for use in some of the revised figures for the secondedition.

A number of publishers and individuals granted us gratispermission for the use of material adapted from their publica-tions. These include Elsevier, W. H. Freeman and Company, S.Karger AG, Basel, The Johns Hopkins University Press, The Uni-versity of Chicago Press Ms. Elizabeth Rugh Downs, Dr. DaphneSoares, McGraw-Hill, Akademie Verlag, The Royal Society of

London, The Cambridge University Press, Thomson Learning,and John Wiley & Sons. We thank them for their generosity andthe support of scholarly endeavors that it demonstrates.

We offer our special thanks to several additional people,who are both friends and colleagues, and who had importantinfluences on various aspects of the writing of this book. Thefirst is Trev Leger, formerly of John Wiley & Sons, who playeda major role in the inception of the first edition many years ago.We also thank the several editors at Wiley-Liss—Kelly Franklin,Ginger Berman, Fiona Stevens, Luna Han, Thomas Moore, andDanielle Lacourciere—who have helped and encouraged usover the years. We also wish to thank Dean Gonzalez for hisexcellent work on the figure reproductions. Next, our friendand colleague, Boyd Campbell, who also contributed to theinception of the book, advised us on many occasions, andoffered numerous valuable suggestions about the overall con-ception and scope of the work. Arthur Popper, another friendand colleague, was instrumental in forming the partnershipbetween us for the task of writing the book. His seeminglymodest proposal had major consequences. Ann Butler espe-cially acknowledges and thanks Harold Morowitz, James Olds,and Robert Smith for their unflagging encouragement andsupport at the Krasnow Institute for Advanced Study and theDepartment of Psychology at George Mason University. Like-wise, William Hodos acknowledges and thanks William S. Hallfor his generous support and encouragement in the Depart-ment of Psychology at the University of Maryland. Finally, eachof us also wishes to thank the other—for much intellectualstimulation, for mutual support, and, most important, for man-aging to remain friends, even through two editions of thisbook!

Acknowledgments

xix

Box 1-1. Morphogenetic Fields and the New “Evo-Devo” Synthesis 7

Box 1-2. Field Homology 10

Box 2-1. Dome Pressure Receptors 33

Box 2-2. Another Taste System? 38

Box 2-3. Isomorphic Topographic Maps 44

Box 3-1. What Is “Neo”About Neocortex, and What Is “Iso”About Isocortex? 58

Box 4-1. Hagfishes: Invertebrate Chordate or Legitimate Vertebrate? 75

Box 4-2. The Early Divergence of Synapsids 81

Box 4-3. Turtles: Welcome Home to Diapsid-ville! 82

Box 5-1. Did the Dinosaurs Have Small Brains? 103

Box 5-2. A New Taxonomic Method Based on BrainAllometry 104

Box 5-3. Are There Constraints on Brain Growth? 106

Box 5-4. Brain Evolution and Consciousness 107

Box 8-1. Neuroactive Substances in the Spinal Cord 142

Box 8-2. A Neuroendocrine Organ in the Spinal Cord: The Caudal Neurosecretory System 145

Box 8-3. Sexual Dimorphism in the Spinal Cord 151

Box 11-1. The Marvelously Versatile Trigeminal Nerve 187

Box 12-1. The Unusual Abducens Nucleus of Goldfish: A General Somatic Efferent Nucleus “Gone Walkabout” 216

Box 12-2. The Ciliary Muscles of Diving Birds:A Magnificent Adaption 217

Box 13-1. Neuroactive Substances and Sleep 235

Box 13-2. Constant Vigilance and Unihemispheric Sleep 237

Box 14-1. Lugaro Cells and Unipolar Brush Cells 254

Box 14-2. Is There More Than One Cerebellum in the Brain? 258

Box 14-3. Myelinated Dendrites in the ElectrosensoryLateral Line Lobe of Mormyrids 260

Box 18-1. Magnetoreception and the Optic Tectum 313

Box 18-2. Tectal Ganglion Cells With Bottlebrush Dendritic Endings: Questions About TectalLamination 332

Box 21-1. A Strange Nucleus in Some Ray-Finned Fishes 413

Box 22-1. Evolutionary Origin of the Lemnothalamic Visual Pathway: New Perspectives 433

Box 23-1. Hypothalamic Peptides and Proteins 448

Box 25-1. Evolution of Sensory Cortices Across Mammals 505

Box 25-2. Complex Cognitive Functions of Parietal and Prefrontal Cortical Areas in Humans 506

Box 25-3. The Impressive Cognitive Abilities of Birds 514

Box 26-1. Evolution of the Skull and Evolution of Frontal Vision 524

Box 26-2. Functional Streams in the Avian TectrofugalPathway 542

Box 27-1. What Is “Neo”About the Neospinothalamic Tract? 553

Box 28-1. Sexual Dimorphism in the Auditory and Vocal Control Systems 586

Box 29-1. The Olfactory and Vomeronasal Systems of Snakes604

Box 30-1. The Hippocampus and the Amygdala of Goldfish 616

Box 30-2. Imaginative Images of the Hippocampus 618

Box 31-1. Eyes, Eye Evolution, and Pax-6 642

List of Boxes

xxi

Part One

EVOLUTION AND THEORGANIZATION OF THE CENTRALNERVOUS SYSTEM

INTRODUCTION

One of the primary fascinations of the natural world is thevast diversity of living organisms within it. Diversity of organ-isms and their many body parts is a hallmark of biology. Bio-logical diversity has been produced by the process of naturalselection, part of which is a reflection of changing climates,geophysical phenomena, and habitats. The pressures of naturalselection act on spontaneous variations of the phenotypes thatoccur within a population and are the result of mutationalchanges within the genes.

For the study of biological diversity, we need to recognizethe natural groupings to which individual organisms belong.A species is usually defined as a naturally interbreeding set of individual organisms or set of populations of organisms.The English words “species” and “special” derive from the same Latin term specialis, and in fact each species is distin-guished by its particular, special feature(s) that is/are unique toit.The next level of phylogenetic classification is that of genus,which is a set of species that are more closely related to each other than to species outside the genus. Additional exam-ples of levels are those of family, order, class, and phylum.Also, various intermediate levels, such as subfamily, infraorder,supraorder, and so on, are employed as appropriate. Evenwithin a species, various subspecies can be recognized. Theterm taxon applies to any defined, natural group of organisms,such as a species, order, or class. The term clade can also beused to refer to such defined natural groups. The terms taxonand clade are usually and best used to apply to monophyleticgroups, which are groups that include all of the descendantsof a specified common ancestor and no other members. In

practice, often only the extant (living) descendants areaddressed.

Our current understanding of biological diversity beganwith the theory put forth by Charles Darwin (and independ-ently by Alfred Russel Wallace) in 1858–1859.This theory statesthat a process of evolution by natural selection has producedthe variation that is documented by the fossil record andamong extant species. The source of the variation upon whichnatural selection acts was not identified until the science ofgenetics was established by the pioneering work of GregorMendel, who in 1865 formulated the principle of particulateinheritance by the means of transmitted units or genes, and thelater work of Theodosius Dobzhansky and others in the firsthalf of the twentieth century.

Modern evolutionary theory embodies the work of Darwinin the context of genetics, molecular biology, and other rele-vant sciences. This interrelationship of disciplines was termedan evolutionary synthesis by Julian Huxley in 1942; it refersto the recognition that both gradual evolutionary changes and larger evolutionary processes, such as speciation, areexplainable in terms of genetic mechanisms. Since that time,a substantial body of work in genetics, systematic biol-ogy, developmental biology, paleontology, and related fields has yielded new and more complex insights on this sub-ject. The title of a recent book by Niles Eldredge (1985), Un-finished Synthesis, reflects the continuing debate within thefield.

Until Darwin’s publication of his views, most Western sci-entists believed that most or all species of wild animals livingat that time had been unchanged since their creation by a deity.Darwin’s idea that living creatures had evolved over longperiods of time was accepted fairly readily. Some resisted the

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1Evolution and Variation

Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, Second Edition, by Ann B. Butler and William Hodos.Copyright © 2005 John Wiley & Sons, Inc.

4 E VO L U T I O N A N D VA R I AT I O N

idea of humans being animals in continuity with nature, thatis, that humans are related to any other animals, such as apesand monkeys. That evolution is a directionless process employ-ing natural selection is a concept that has been accepted bysome but resisted with vigor by others, even today.

The idea that evolution is progressive in the sense thatprogress or continuous improvement occurs over time isseductive and comforting. It is seductive in its appeal to theegocentricity of our species and comforting as a source ofmoral principles. The Aristotelian concept of a scala naturaethat living animals can be arranged in a continuous, hierarchi-cal, ladder-like progression with humans at the pinnacleembodies this appeal, as does the Judeo–Christian tradition ofcreation that culminates with the human species. Julian Huxleypromoted the idea that, although evolution was withoutpurpose, it was progressive. He believed that ethical principlesand the meaning of human existence could be derived fromthe position of humans at its pinnacle.

The scala naturae concept of progressively ascendingscales of life forms, such as the fish–frog–reptile–rat–cat–monkey–human sequence, is seen as intuitively correct. The pervasive flaw in all such rankings is that they are made from ananthropocentric point of view. The anthropocentric scale,however, is of no greater scientific value in an evolutionarycontext than one based, for example, on our assessment of the animals’ beauty. The appeal of the idea of progress over evolution is based on the fact that progress itself, like beauty,is a human concept and value; it is not, however, a biological principle.

Inherent in the notion of a scale of nature is the idea thateach animal has a natural rank on this scale. The more“advanced”animals (humans and the ones seemingly closest tohumans) occupy ranks high on the scale, and those that seemto bear less resemblance to humans are relegated to the lowerranks. Thus, we have come to refer to some animals as “thehigher vertebrates”and others as “the lower vertebrates,”or “thesubmammalian vertebrates.” Unfortunately, terms like “higher,”“lower,” and “submammalian” represent only homocentric value judgments; they are thus inappropriate ways of com-paring animals and have no place in the vocabulary of evolu-tionary biology. Many extant species of vertebrates are onlydistantly related to humans and resemble them very little;nevertheless, these animals are just as successful and welladapted to their environments as humans and their closest relatives are to their own environments. The simple fact thatanimals are different does not confer any rank to them relativeto each other.

Many humans consider the human species as “special,” dif-ferent in some way and standing apart from all other species.As noted above, the word “special” and “species” are derivedfrom the same Latin term, so in that sense, all species arespecial.Thus, to the extent that we are a species, we are specialby definition. The perspective of William S. Gilbert and SirArthur Sullivan, in their operetta The Pirates of Penzance, is rel-evant here: “If everybody’s somebody, then no one’s anybody.”Scala naturae thinking that views any one species as superiorto all others is in fact one of the greatest impediments to under-standing the biological world and to appreciating the place ofour own species within it. Evolution does not create superiorand inferior taxa; it simply creates diversity.

DIVERSITY OVER TIME

Biological diversity is a result of natural selection actingon random variations within populations of organisms. Thedegree of biological diversity has increased over time in someways. For example, twice as many species of marine animals(invertebrate and vertebrate) exist today as existed in the Pale-ozoic era. In other ways, however, biological diversity has dra-matically decreased over time. In the Paleozoic era, the numberof groups of higher taxonomic rank (more inclusive categories)was far greater than the number that exists today. Diversity inthe range of basic body plans has decreased, whereas the diver-sity of species having any of the few, extant, basic body planshas increased.The greater number of extant species is groupedwithin the fewer number of higher categories.

One explanation for this more complex pattern of evolu-tionary change focuses on processes that tend to eliminateextremes in variation, such as competition under conditions ofnatural selection. Animals with the more successful body planswould ultimately survive, and the number of higher categoriesthus decreases over time. A second explanation involves therandom process of extinction. To consider this possibility, weneed to examine evolutionary history in terms of the extremephysical forces that shape it.

Extinctions of varying degree repeatedly occur and pro-foundly affect biological evolution. Some extinctions are ofmodest degree and limited extent, happening to isolated pop-ulations due to normal environmental fluctuations or acciden-tal factors. Species most resistant to environmental fluctuationstend to be those with individuals that have larger bodies, longerlives, and a greater degree of social interaction related to breed-ing behaviors. Other extinctions are of greater consequenceand related to habitat fragmentation caused by such factorsas tectonic shifts, temperature changes, alteration in rainfallpatterns, and changes in oceanic level. When habitat fragmen-tation occurs, species more resistant to extinction are thosethat are herbivorous versus carnivorous and, among carnivores,of smaller body size. Those species with more strictly definedhabitat requirements—habitat specialists—are more proneto extinction than species that are habitat generalists.Species with populations of smaller size or lesser density arelikewise more prone to extinction than those of greater sizeand/or density.

Of the greatest consequence are mass extinctions of hun-dreds or thousands of species, such as those that occurred atthe end of the Permian and the Cretaceous periods. Not onlyare mass extinctions dramatic and of momentous impact onbiological flora and fauna, but they appear to occur with aregular periodicity. Mass extinctions have recurred on a cycleof about 26 million years for at least the last 225 million years.The Cretaceous extinction occurred 65 million years ago. Toaccount for a cycle on such a long time scale, extraterrestrialcauses, such as asteroid or comet impacts, have been consid-ered, and evidence from the distribution of iridium, a relativelyrare element of extraterrestrial (meteoritic) origin, in theearth’s surface supports this possibility.A recurring disturbanceof the Oort cloud—the cloud of comets that circle the sun—could release comets that could then impact the earth with cat-astrophic results.

E VO L U T I O N A RY M E C H A N I S M S 5

In mass extinctions, some species and groups of specieshave better chances of survival than others. Categories of taxathat have a greater number of species (species-rich clades)tend to be composed of habitat specialist species, species thathave become specialized for survival in a particular habitat,which are thus more susceptible to extinction if the habitatchanges suddenly. In contrast, the habitat generalist speciestend to be in taxonomic categories with a fewer number ofspecies (species-poor clades), have wider geographic ranges,and can more readily shift habitats if conditions change.

In normal times, species-rich clades undergo a net increasein species number, offsetting losses due to limited environ-mental fluctuations, accidents, and habitat fragmentation. Thisspeciation has a pattern of punctuated equilibrium—rapidchange followed by a longer period of little or no change, asdiscussed below. Species-poor clades, on the other hand, havea lower rate of speciation but are more resistant to environ-mental and habitat assaults. This balance permits both types ofclades to flourish in the intervals between mass extinctions. Inmass extinctions, the species-rich clades are more vulnerable,and thus over time, fewer higher categories survive. Morespecies arise in at least some of the remaining higher categoriesdue to new waves of speciation following each period of massextinction. Biological evolution is thus the net result of multi-ple independent processes.

EVOLUTIONARY MECHANISMS

Evolution can be defined simply as a change over time. Inbiological systems, random genetic variation occurring withina population allows for phenotype variation, which naturalselection can then act upon. Darwin recognized that evolutionoccurs as a consequence of two separate processes. The firstprocess, which we know today to encompass mutations andgenetic recombinations as well as other factors, is a randomprocess that produces variability. The second process, naturalselection, is not random but rather opportunistic, and it actson this variability. Natural selection acts on populations, affect-ing the frequency of particular genes within the population,rather than on individuals.

Genetic FactorsMutations and changes in the frequency of certain gene

alleles, that is, alternate forms of the gene (dominant vs. reces-sive), account for diversity within an interbreeding population.The individual members of the population are similar but notidentical. Because a gene may exist in a large variety of allelicforms but an individual animal has only one pair of alleles foreach gene, any given individual possesses only a small fractionof the total genetic variation that is stored in the population asa whole.

The relative frequencies of alternative alleles and geno-types reach equilibrium and then tend to remain constant in alarge, randomly mating population. Despite this tendency,changes in the frequencies of different alleles do occur oversucceeding generations. In addition to mutations, factors thataffect the frequency of alleles in a species include geneticrecombination, gene flow, and isolating mechanisms.

Gene recombination assembles an existing array of allelicforms of different genes into a variety of combinations. Thisdoes not increase the frequencies of these alleles but doesincrease variability. While mutation is the ultimate source ofgenetic variation, recombination generates numerous geno-typic differences among individuals in a population. Conse-quently, recombination provides a large number of thevariations acted upon by natural selection.

Gene flow is a change in the frequency of particular allelescaused by individuals of the same species migrating into andinterbreeding within a given population. Gene flow is essentialto maintaining various populations as members of a singlespecies, since the most important aspect of the definition of aspecies is that it consists of a set of populations that actuallyor potentially interbreed in nature. Gene flow is responsible forgenetic cohesion among the various populations that form thespecies. This process is a stabilizing influence on genetic vari-ation and is responsible for the relatively slow rate of evolutionthat occurs in common, widespread species.

Biological mechanisms that isolate one population fromanother reproductively are in direct contrast to gene flow anddefine the limit of the species. Geographic isolation, such asislands separated from each other by the ocean or a peninsulabeing isolated as an island due to a rise in the level of the ocean,can result in changes in gene frequencies between the twopopulations. A small number of individuals that becomes iso-lated from the rest of the population will not necessarily havethe same alleles in the same frequency distribution as thewhole original population, resulting in a shift in allelic fre-quencies in the isolated population. Examples of such isolatedpopulations are various species of birds on various islands inthe Galapagos, Hawaiian, and other similar island groups. If thegeographic isolation eventually ceases, reproductive isolationmay nevertheless be maintained by newly established mechan-ical incompatibilities of the male and female or by behavioralisolation caused by differences in mating ritual or speciesrecognition cues that exclude some formerly potential mates.

Natural SelectionNatural selection acts on the variability and establishes

certain variant types in new frequencies within a given popu-lation. Natural selection is the increase in frequency of partic-ular alleles as a result of those alleles enhancing thepopulation’s ability to survive and produce offspring. Thefitness of a variant is a measure of how strongly the variantwill be selected for, that is, how adaptive it is. Thus, a novelvariant that enables a population to capitalize on a vacant nichemay rapidly establish itself. Alternatively, selective pressuresthat are too strong, such as a relatively sudden decrease inambient temperatures during an ice age, may result in extinc-tion of populations. In such a case, the variability within thepopulation is simply not extensive enough to fortuitously havethe number of variants that would allow for selection of adap-tations to the cold.

If a mutant allele appears infrequently in a large popula-tion, the initial frequency of the allele will be low and will tendto remain low. If a mutant allele appears in a single individualand has no selective advantage or disadvantage, it can bychance alone readily become extinct. On the other hand, if it

6 E VO L U T I O N A N D VA R I AT I O N

even slightly enhances the ability of its bearer to live and reproduce, it will increase in frequency. Selection is the mostimportant means by which allele frequencies are changed.Natural selection can be considered to consist of the differen-tial, nonrandom reproduction of particular alleles. As alleles areparts of whole genotypes, selection can also be thought of asthe differential and nonrandom reproduction of particulargenotypes.

Darwin considered natural selection to mean differentialmortality. Contemporary evolutionists look upon it as differen-tial reproduction. Although natural selection does frequentlytake the form of differential mortality, other strategies occur aswell, such as increasing the number of offspring produced orimproving the chance of successful mating by increasing efficiency in getting food or evading predators. Differentialmortality can be regarded as one form of differential repro-duction, if, for example, some animals do not survive longenough to reproduce.

Gene alleles most often have multiple effects, that is, theyare pleiotropic. Some of the characteristics determined by anallele may be advantageous to the individual, while others maybe disadvantageous. An individual carrying an allele (A) mighthave a selective advantage over another individual carrying itsmatching allele (A¢), but might be inferior to the phenotype ofthe second individual in some other character produced byallele A. If individuals carrying the allele A have a net superi-ority over individuals carrying the allele A¢, then allele A willincrease in frequency despite its deleterious side effects.

The discussion thus far has been primarily concerned withselection of single alleles, but the same principles can beextended to encompass combinations of two or more genes.Many adaptations are based not on single genes but on multi-ple genes or gene combinations and the resultant phenotypeon which selection acts. Populations of organisms exist in aparticular environment to which they must be fitted or adaptedin order to live and reproduce successfully. If the environmentremains stable and the population is highly adapted, selectionoperates primarily to eliminate peripheral variants and off-types that arise by mutation or recombination. If a changeoccurs in the environment, one or more of the peripheral vari-ants may be better adapted to the new conditions than thosewith the more normal genotype. Selection now takes a differ-ent form, favoring the formerly peripheral variants and elimi-nating some of the standard genotypes.

Since natural selection acts on a population rather thanany individual, traits such as “altruism” can be selected for. Forexample, in many species, an individual animal may do workor even sacrifice itself in the service of offspring that are relatedbut not its own. By so doing, the animal is protecting the genesthat it has in common with those offspring. Thus, rather thanbeing truly altruistic, such acts are actually self-serving in thatthey are a mechanism to protect at least some genes that arethe same as the animal’s. The genetic basis for the potential toact in support and defense of related offspring is thus likely tobe retained in the population.

Darwin believed that the course of evolution resulted pri-marily from natural selection acting on variations within pop-ulations. In his view, this process produced gradual changesthat could, over long periods, account for all the organic diver-sity that we observe today. The modern synthesis has incorpo-

rated the new knowledge of mechanisms provided by genet-ics, including that from the recent advances in molecularbiology. Nevertheless, emphasis is still placed on the role ofnatural selection acting at the level of the population, asadvanced by Darwin. The term microevolution refers to suchdivergences of populations within a given species, resulting inraces or breeds. Microevolution involves the gradual accumu-lation of small changes over time, the way Darwin envisionedthe evolutionary process. Another type of gradual evolutionarychange is phyletic evolution (also called anagenesis). Inphyletic evolution, a single lineage, without branching intodivergent lineages, undergoes change over time. The ancestraland descendant portions of the lineage can become sufficientlydifferent that they are recognized as different species.

In 1972, Niles Eldredge and Stephen Jay Gould, after exam-ining evidence from the fossil record of marine invertebrates,pointed out that in this group at least, few examples exist ofspecies that undergo significant change gradually through time.In most cases, a particular morphology is retained for millionsof years and then changes abruptly over a short period of time.Eldredge and Gould used the term punctuated equilibriumto describe this pattern. Punctuated equilibrium is similar tothe concept of saltatory evolution, the sudden origin of newtaxa by abrupt evolutionary change, held by some of the nine-teenth century biologists. The process by which new taxa areformed, from the specials level on up through the higher taxiccategories, is called macroevolution. The formation of newspecies can also be referred to as speciation or cladogene-sis. The term speciation is used to describe a process in whicha single species gives rise to a branch that becomes establishedas a new, sister species or splits into two new lineages that bothbecome new species, that is, are reproductively isolated fromeach other.

Darwin and a number of other biologists thought that themicroevolutionary process of gradual morphological changebrought about by the accumulation of genetic mutations couldalso explain the origin of the so-called higher taxonomic cate-gories of species, families, orders, and classes. However, themorphological differences between various orders and fami-lies, and even those that distinguish individual species withina genus, can be considerable. After all, morphological differ-ences are the major basis for defining these various higher cat-egories. The new synthesis of evolution and developmentalbiology that is now underway reemphasizes macroevolution-ary events and their crucial significance for evolutionary diver-gences and the formation of new taxa. Changes in thedevelopmental process—such as heterochrony, a change inthe relative timing of potentially related developmental events,and allometric alterations, a change in the proportional growthof a structure and/or its elements—can have dramatic effectson the phenotype. Such changes in the developmental processintervene between genotype and adult phenotype and canproduce the types of substantial and rapid morphologicalchanges that typify saltatory evolutionary events. As discussedin Box 1-1, these kinds of changes involve developmentalfields, also called morphogenetic fields, embryonic fields,or anlagen (singular: anlage), which are the fundamental evolutionary units of macroevolutionary change. Darwinhimself recognized the crucial interrelationship of embryologyand evolution.

comparative vertebrate neuroanatomy evolution and …€¦ · vertebrates—anatomy. 3. nervous...

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