Developmental SCOTT F. GILBERT BiologySWARTHMORE COLLEGE

Preface xii

PART I :PATTERNS OF DEVELOPMENT

Chapter 1 :An introduction to animal development

3

Introduction

4

Origins of sexual reproduction

1 5Principal features of development

4

Colonial eukaryotes : The evolution o fOur eukaryotic heritage

7

differentiation

1 9Development among the unicellular

The Volvocales

1 9eukaryotes

10

Dictyostelium

23Control of developmental

Developmental patterns among metazoans

26morphogenesis in Acetabularia

10

Protostomes and deuterostomes

26Differentiation in the amoeboflagellate

Naegleria

1 3

Chapter 2 :Fertilization : beginning a new organism

31

Introduction

32

Gamete fusion and prevention o fStructure of the gametes

32

polyspermy

5 0Sperm

32

Fusion between sperm and oocyte cellEgg

36

membranes

50Recognition of sperm and egg : Action at a

Prevention of polyspermy

5 3distance

40

Fusion of the genetic material

58Sperm attraction

40

Early responses

6 3The acrosome reaction

41

Late responses

6 5Recognition of sperm and egg : Contact of

Rearrangement of egg cytoplasm

66gametes

44

Sidelights & Speculations : The nonequivalence ofSpecies-specific recognition in sea

mammalian pronuclei

6 1urchins

44

Activation of egg metabolism

62Gamete binding in mammals

47

Chapter 3 :Cleavage: creating multicellularity

73

introduction

74

Sidelights & Speculations : The cell surface andPATTERNS OF EMBRYONIC CLEAVAGE

75

the mechanism of compaction

94Radial holoblastic cleavage

77

Formation of the inner cell mass

94The sea cucumber, Synapta

77

Sidelights & Speculations : Twins

97Sea urchins

78

Meroblastic cleavage types

98Amphibians

82

Discoidal cleavage

98Spiral holoblastic cleavage

84

Superficial cleavage

98Bilateral holoblastic cleavage

88

MECHANISMS OF CLEAVAGE

102Rotational holoblastic cleavage

89

Summary

107

Chapter 4 :Gastrulation: reorganizing the embryonic cells

110

Introduction: General features of

Cell movements and construction of thegastrulation

111

archenteron

12 6Sea urchin gastrulation

112

Epiboly of the ectoderm

13 0Ingression of primary mesenchyme

112

Gastrulation in birds

13 1First stage of archenteron invagination

116

Overview of avian gastrulation

13 1Second stage of archenteron

Mechanisms of avian gastrulation

13 7invagination

117

Gastrulation in mammals

139Amphibian gastrulation

118

Overview of mammalian gastrulation

139Cell movements during amphibian

Sidelights & Speculations : The roles of thegastrulation-an overview

118

chorion

144End of the blastula stage and

positioning of the blastopore

122

Chapter 5:Early vertebrate development : neurulation and ectoderm

149

The vertebrate pattern of development

150

Development of the eye

17 2Neurulation

152

The neural crest and its derivatives

17 8The neural tube and the origins of the

Sidelights & Speculations : The mechanism forcentral nervous system

155

neural crest migration

183Mechanism of neural tube formation

158

Pluripotentiality of neural crest cells

183Differentiation of the neural tube

159

The epidermis and the origin of cutaneou sSidelights & Speculations : The evolution of

structures

184cerebral development

165

Cutaneous appendages

18 6

Chapter 6 :Early vertebrate development: mesoderm and endoderm

190

Introduction

191

Sidelights & Speculations : Differentiation an dMESODERM

191

the cell cycle

201

Dorsal mesoderm: Differentiation of somites 191

Osteogenesis : Development of bones

202Myogenesis : Differentiation of skeletal

Lateral plate mesoderm

204muscle

196

Formation of extraembryonic membranes

205

Heart and circulatory system

208

Sites of hematopoiesis

222The heart

208

ENDODERM

223Formation of blood vessels

209

Pharynx

223Sidelights & Speculations : Redirecting blood flow

The digestive tube and its derivatives

226at birth

216

Liver, pancreas, and gallbladder

227Sidelights & Speculations : Tumor-induced

The respiratory tube

228angiogenesis

216

Sidelights & Speculations : Teratocarcinoma

229Development of blood cells

21 8Pluripotential stem cells and

hematopoietic microenvironments

21 8

PART II :MECHANISMS OF CELLULAR DIFFERENTIATION

Chapter 7 :Progressive determination

237

Introduction

238

Hans Spemann and Hilde Mangold :

Preformation and epigenesis

238

Primary embryonic induction

25 9

August Weismann : The germ-plasm theory 241

Regional specificity of induction

260Wilhelm Roux: Mosaic development

243

Sidelights & Speculations : The mechanism ofHans Driesch : Regulative development

244

primary embryonic induction

26 3

Sven Hörstadius: Potency and oocyte

Competence and secondary induction

265gradients

24 7Hans Spemann : Progressive determinatio n

of embryonic cells

25 4

Chapter 8 :Determination by cytoplasmic specification

269

Cytoplasmic specification: Mosaic

Sidelights & Speculations : Intracellula rdevelopment

270

localization and movements of

Cytoplasmic specification in tunicate

morphogenic determinants

276

embryos

270

Cytoplasmic localization in mollusc embryos 277

Cytoplasmic localization of germ cell

Germ cell determination in amphibians 28 8

determinants

281

The nature of cytoplasmic determinants

29 0Germ cell determination in nematodes

281

Summary

29 3Germ cell determination in insects

283

Chapter 9 :

Genomic equivalence and differential gene expression : embryological investigations

297

Introduction

298

Amphibian cloning : Restriction of cell

Genomic equivalence

298

potency

30 5

Transdetermination

300

Amphibian cloning : Exceptions to restriction 308

Metaplasia

300

Sidelights & Speculations : Cloning

314

Chapter 10:Genomic equivalence and differential gene expression: molecular investigations

318

Introduction

319

Changes in lymphocyte genes

329Molecular biology techniques : Nucleic acid

Sidelights & Speculations : Gene alterations

33 8hybridization and gene cloning

319

Differential RNA synthesis

339Differential gene expression

325

Chapter 11:Transcriptional regulation of gene expression : the nature of eukaryotic genes

348

Introduction

349

RNA polymerase III recognition

36 8Structure of the eukaryotic genome

349

RNA polymerase I recognition

369Structure of eukaryotic chromatin :

Sidelights & Speculations : Promoter structur eNucleosomes

355

and differentiation

370Regulation of gene accessibility on the

DNA methylation

370nucleosome

357

Sidelights & Speculations : Z-DNA andSidelights & Speculations : Transcriptional

nucleosome structure

372regulation by the nuclear matrix

362

Structure of eukaryotic genes : Exons andStructure of eukaryotic genes : RNA

introns

373polymerase recognition sites

362

Mechanism for RNA splicing

379RNA polymerase II recognition

363

Summary

38 1Sidelights & Speculations : Enhancers

36 6

Chapter 12 :Transcriptional regulation of gene expression: transcriptional changes in developing cells 38 6

Introduction

387

Visualization of transcription fro mHeterochromatin

387

amplified genes

397Paternal heterochromatin in meally

Drosophila chorion genes

39 9bugs

387

Selective gene transcription

39 9

Mammalian X chromosome inactivation 389

Chromosomal puffs and lampbrushSidelights & Speculations : Mechanism of X

chromosomes

400chromosome inactivation

393

Ovalbumin synthesis

403Amplified genes

393

Sidelights & Speculations : Coordinated geneAmplification of ribosomal RNA genes

393

expression

407Mechanism of ribosomal gene

Globin gene transcription

40 9amplification

394

Chapter 13 :

Control of development by RNA processing

413

Introduction

414

Control of development by nRNATranscriptional model of developmental

processing

420regulation

414

Sidelights & Speculations : Mechanisms forHeterogeneous nuclear RNA

417

specific nuclear RNA processing

425

Complexity of nuclear and messenger RNAs 419

Evidence for unprocessed messageprecursors in the nucleus

427

Selection of alternative proteins by RNA,

Sidelights & Speculations : Other roles ofprocessing

428

differential RNA processing in antibod yWidespread use of differential RNA

gene regulation

429processing

428

Summary

43 1

Chapter 14:Translational and posttranslational regulation of developmental processes

433

TRANSLATIONAL REGULATION OF

Translational control of casein synthesis

453DEVELOPMENT

434

The widespread use of translationa lMechanism of eukaryotic translation

434

regulation

45 4Translational control of coordinated protein

Sidelights & Speculations : Other types ofsynthesis : Ribosomes and

translational control

45 5hemoglobin

437

POSTTRANSLATIONAL REGULATION O FTranslational control of oocyte messages

441

GENE EXPRESSION

456 .Evidence of maternal regulation of early

Activation of proteins by posttranslationa ldevelopment

441

modifications

456Stored messenger RNA

443

Inactivation of proteins by posttranslationa lCharacterization of maternal messages

447

modifications

456Mechanisms for translational control of

Subcellular localization of proteins b yoocyte messages

448

posttranslational modifications

46 1Maternal mRNA and embryonic

Supramolecular assembly

46. 2cleavage

452

Collagen : An epitome of posttranslationa lSidelights & Speculations : Maternal RNA in

regulation

463mammals

453

PART III :CELL INTERACTIONS IN DEVELOPMENT

Chapter 15 :Spatial development: the role of the cell surface

471

Introduction

472

Sidelights & Speculations : Cell sorting and self-Structure of the cell surface

472

assembly

4. 9 6Cell membrane

472

Sidelights & Speculations : Two systems ofCell membrane changes during

adhesive specificity and thei rdevelopment

477

developmental significance

49 9Extracellular matrix

479

Differential cell affinity in anima lSidelights & Speculations : Oncofetal antigens

480

development

50 0Cell surface modifications

485

Sea urchin gastrulation

504Locomotion

487

The reeler and staggerer mutants of theDifferential cell affinity

489

mouse

502Stationary cultures

489

Cell recognition in vivo : The T-complexRotary cultures

491

of the mouse

504The thermodynamic model of sorting out

493

Sidelights & Speculations : Glycosyltransferase sAdhesive specificity model of sorting out

495

and intercellular recognition

508

Chapter 16 :Proximate tissue interactions : secondary induction

515

Introduction

516

Coordinated differentiation andInstructive and permissive interactions

516

morphogenesis in the pancreas

530Intercellular coordination in proximate

The nature of proximity in epithelio-interactions

518

mesenchymal inductions

53 1

Epithelio-mesenchymal interactions

521

Mechanism of branching in the formation o f

Regional specificity of induction

522

parenchymal organs

537

Genetic specificity of induction

523

Induction of plasma cells

540Sidelights & Speculations : Development and

Sidelights & Speculations : Crosslinking andmacroevolution

525

induction

543Formation of parenchymal organs

526

Induction of the chick limb

547

Chapter 17 :Pattern formation

555

Introduction

556

Specification of positional informatio n

Pattern formation during limb development 556

in imaginal discs

57 6The limb field

557

Pattern formation in the vertebrate nervou sPolarization along the limb axes

558

system

57 9Regeneration of limb tissues

563

Direction of axonal growth

57 9Polar coordinate model of pattern

Mechanisms of synaptic specificity

582

formation

565

Qualitative neuronal differences

58 9Genetics of pattern formation in Drosophila

569

Sidelights & Speculations : Cell surface addressCompartmentalization in insect

markers and lymphocyte migration

590development

569

Development of behaviors

59 1Mutations affecting the number of

Sidelights & Speculations : Morphogenesis bysegments

572

specific cell death

593Mutations affecting segmentation : The

Pattern formation in Hydra and Duglesia :bithorax complex

574

Morphallaxis

594

Sidelights & Speculations : Genetic control ofsegmentation

576

Chapter 18:Cell interactions at a distance : hormones as mediators of development

603

Introduction

604

Hormonal control of insectMetamorphosis : The hormonal reactivation

metamorphosis

622of development

604

Sidelights & Speculations : Precocenes

62 5Amphibian metamorphosis

605

Multiple hormonal interactions in mammaryThe phenomenon of amphibian

gland development

62 6metamorphosis

605

The embryonic stage

62 6Hormonal control of amphibian

Adolescence

62 9metamorphosis

607

Pregnancy

63 0Sidelights & Speculations : Neoteny

615

Puberty as a variation on the theme ofMetamorphosis in insects

616

metamorphosis

63 0. Control of cell proliferation : Chalones

634

Chapter 19:Sex determination

638

Introduction

639

Sidelights & Speculations : The development of

Chromosomal sex determinant in mammals 639

sexual behaviors

65 5The developing gonads

641

Environmental sex determination

65 7

The H-Y antigen

643

Temperature-dependent se x

The H-Y receptor

646

determination in reptiles

65 7

Sidelights & Speculations : The hormone-like

Sidelights & Speculations : The extinction ofeffects of H-Y

649

dinosaurs

65 8

Secondary sex determination

649

Location-dependent sex determinatio n

Chromosomal sex determination in

in Bonellia and Crepidula

65 8

Drosophila

654

Hermaphroditism

66 0

Chapter 20:The saga of the germ line

664

Introduction

665

Oogenesis

678Germ cell formation

665

Oogenic meiosis

678Germ cell migration in amphibians

665

The maturation of the oocyte inGerm cell migration in mammals

667

amphibians

680Germ cell migration in birds and

Sidelights & Speculations : Natura lreptiles

668

parthenogenesis

68 1Meiosis

670

Oogenesis in meroistic insects

68 7Spermatogenesis

673

Oogenesis in humans

69 1Spermiogenesis

676

Sidelights & Speculations : The maintenance andGene expression during sperm

breaking of meiotic arrest

69 6development

67 6

Sources for Chapter-Opening Quotations

703

Author Index

705

Subject Index

712