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Contents
PART I ● Patterns and Processes of Becoming:
A Framework for Understanding Animal Development
1 and Teratology 36
The Making of a Body and a Field
Introduction to Developmental Biology
“How Are You, You?” Comparative Embryology and
the Questions of Developmental Biology 2
The Cycle of Life 7
An animal’s life cycle 7
A flowering plant’s life cycle 8
Example 1: A Frog’s Life 8
Gametogenesis and fertilization 9
Cleavage and gastrulation 9
Organogenesis 11
Metamorphosis and gametogenesis 11
Example 2: Even a Weed Can Have
a Flower-Full Life 12
Reproductive and gametophytic phases 12
Embryogenesis and seed maturation 12
Vegetative phases: From sporophytic growth
to inflorescence identity 14
An Overview of Early Animal Development 14
Patterns of cleavage 14
Gastrulation: “The most important time
in your life” 17
The primary germ layers and early organs 17
Understanding cell behavior in the embryo 19
A Basic Approach to Watch Development 20
Approaching the bench: Find it, lose it, move it 20
Direct observation of living embryos 21
Dye marking 22
Genetic labeling 23
Transgenic DNA chimeras 24
Evolutionary Embryology 25
Understanding the tree of life to see
our developmental relatedness 28
The developmental history of land plants 32
Personal Significance: Medical Embryology
Genetic malformations and syndromes 36
Disruptions and teratogens 36
Coda 37
1
2
Specifying Identity
Mechanisms of Developmental Patterning 39
Levels of Commitment 40
Cell differentiation 40
Cell fate maturation 40
Autonomous Specification 41
Cytoplasmic determinants and autonomous
specification in the tunicate 42
Conditional Specification 44
Cell position matters: Conditional specification
in the sea urchin embryo 45
Syncytial Specification 48
Opposing axial gradients define position 49
3
Differential Gene Expression
Mechanisms of Cell Differentiation 55
Defining Differential Gene Expression 56
A Quick Primer on the Central Dogma 56
Evidence for Genomic Equivalence 57
Anatomy of the Gene 59
Chromatin composition 59
Exons and introns 60
Major parts of a eukaryotic gene 61
viii   
Contents
The transcription product and how it is processed 62
Noncoding regulatory elements: The on, off, and
dimmer switches of a gene 62
Mechanisms of Differential Gene Expression:
Transcription 67
Epigenetic modification: Modulating access to genes 67
Transcription factors regulate gene transcription 72
The gene regulatory network: Defining
an individual cell 78
Mechanisms of Differential Gene Expression:
Pre-messenger RNA Processing 79
Creating families of proteins through alternative
pre-mRNA splicing 80
Mechanisms of Differential Gene Expression:
mRNA Translation 82
Differential mRNA longevity 82
Stored oocyte mRNAs: Selective inhibition of
mRNA translation 83
Ribosomal selectivity: Selective activation of
mRNA translation 84
microRNAs: Specific regulation of mRNA translation
and transcription 84
Control of RNA expression by cytoplasmic
localization 87
Mechanisms of Differential Gene Expression:
Posttranslational Protein Modification 88
Coda 95
4 Meristem cells of the Arabidopsis thaliana embryo
Cell-to-Cell Communication
Mechanisms of Morphogenesis 99
A Primer on Cell-to-Cell Communication 100
Adhesion and Sorting: Juxtacrine Signaling and
the Physics of Morphogenesis 101
Differential cell affinity 101
The thermodynamic model of cell interactions 103
Cadherins and cell adhesion 103
The Extracellular Matrix as a Source of
Developmental Signals 106
Integrins: Receptors for extracellular matrix
molecules 108
The Epithelial-Mesenchymal Transition 108
Cell Signaling 109
Induction and competence 109
Paracrine Factors: Inducer Molecules 114
Morphogen gradients 114
Signal transduction cascades: The response
to inducers 116
Fibroblast growth factors and the RTK pathway 116
FGFs and the JAK-STAT pathway 118
The Hedgehog family 119
The Wnt family 123
The TGF-β superfamily 126
Other paracrine factors 127
The Cell Biology of Paracrine Signaling 132
Focal membrane protrusions as signaling sources 134
Juxtacrine Signaling for Cell Identity 137
The Notch pathway: Juxtaposed ligands and receptors
for pattern formation 137
Paracrine and juxtacrine signaling in coordination:
Vulval induction in C. elegans 138
5
Stem Cells
Their Potential and Their Niches 143
The Stem Cell Concept 144
Division and self-renewal 144
Potency defines a stem cell 145
Stem Cell Regulation 146
Pluripotent Cells in the Embryo 148
and beyond 148
Cells of the inner cell mass in the mouse embryo 151
Adult Stem Cell Niches in Animals 153
Stem cells fueling germ cell development in
the Drosophila ovary 153
Adult Neural Stem Cell Niche of the V-SVZ 155
The neural stem cell niche of the V-SVZ 155
The Adult Intestinal Stem Cell Niche 160
Clonal renewal in the crypt 161
Stem Cells Fueling the Diverse Cell Lineages
in Adult Blood 162
The hematopoietic stem cell niche 163
The Mesenchymal Stem Cell: Supporting a Variety
of Adult Tissues 165
Regulation of MSC development 166
The Human Model System to Study Development
and Disease 167
Pluripotent stem cells in the lab 167
Induced pluripotent stem cells 170
Organoids: Studying human organogenesis
in a culture dish 173

PART II ● Gametogenesis and Fertilization: The Circle of Sex
6 7
Sex Determination and Gametogenesis 179
Sex Determination 179
Chromosomal Sex Determination 180
The Mammalian Pattern of Sex Determination 180
Gonadal sex determination in mammals 182
Secondary sex determination in mammals:
Hormonal regulation of the sexual phenotype 186
Chromosomal Sex Determination in Drosophila 191
Sex determination by dosage of X 191
The Sex-lethal gene 191
Doublesex: The switch gene for sex determination 193
Environmental Sex Determination 195
Gametogenesis in Animals 196
PGCs in mammals: From genital ridge to gonads 197
Meiosis: The intertwining of life cycles 199
Spermatogenesis in mammals 202
Oogenesis in mammals 204
Sex Determination and Gametogenesis
in Angiosperm Plants 206
Sex Determination 206
Gametogenesis 209
Pollen 211
The ovule 211
PART III ● Early Development: Cleavage, Gastrulation, and Axis Formation
8 and ctenophores 248
Snails, Flowers, and Nematodes
Different Mechanisms for Similar Patterns
of Specification 247
A Reminder of the Evolutionary Context That
Built the Strategies Governing Early
Development 248
Contents   ix
Fertilization Beginning a New Organism 215
Structure of the Gametes 216
Sperm 216
The egg 218
Recognition of egg and sperm 221
External Fertilization in Sea Urchins 221
Sperm attraction: Action at a distance 221
The acrosome reaction 223
Recognition of the egg’s extracellular coat 224
Fusion of the egg and sperm cell membranes 224
Prevention of polyspermy: One egg, one sperm 224
Activation of egg metabolism in sea urchins 228
Fusion of genetic material in sea urchins 233
Internal Fertilization in Mammals 234
Getting the gametes into the oviduct:
Translocation and capacitation 234
In the vicinity of the oocyte: Hyperactivation, directed
sperm migration, and the acrosome reaction 236
Recognition at the zona pellucida 236
Gamete fusion and the prevention of polyspermy 237
Activation of the mammalian egg 239
Fusion of genetic material 239
Fertilization in Angiosperm Plants 241
Pollination and beyond: The progamic phase 241
Pollen germination and tube elongation 242
Pollen tube navigation 242
Double fertilization 243
Coda 244
The diploblastic animals: Cnidarians
The triploblastic animals: Protostomes
and deuterostomes 248
What’s to develop next 250
Early Development in Snails 250
Cleavage in Snail Embryos 251
Maternal regulation of snail cleavage 252
Axis determination in the snail embryo 259
Gastrulation in Snails 262
x   
Contents
The Nematode C. elegans 263
Cleavage and Axis Formation in C. elegans 264
Rotational cleavage of the egg 264
Anterior-posterior axis formation 265
Dorsal-ventral and right-left axis formation 266
Control of blastomere identity 267
Gastrulation of 66 Cells in C. elegans 270
9 Fate maps and the determination
The Genetics of Axis Specification
in Drosophila 273
Early Drosophila Development 275
Fertilization 275
Cleavage 276
The mid-blastula transition 277
Gastrulation 278
The Genetic Mechanisms Patterning
the Drosophila Body 281
Segmentation and the Anterior-Posterior
Body Plan 282
Maternal gradients: Polarity regulation
by oocyte cytoplasm 283
The anterior organizing center: The Bicoid and
Hunchback gradients 286
The terminal gene group 287
Summarizing early anterior-posterior axis
specification in Drosophila 288
Segmentation Genes 288
Segments and parasegments 288
The gap genes 289
The pair-rule genes 291
The segment polarity genes 292
The Homeotic Selector Genes 295
Generating the Dorsal-Ventral Axis 297
Dorsal-ventral patterning in the oocyte 297
Generating the dorsal-ventral axis
within the embryo 298
Axes and Organ Primordia: The Cartesian
Coordinate Model 299
10
Sea Urchins and Tunicates
Deuterostome Invertebrates 303
Early Development in Sea Urchins 304
Early cleavage 304
Blastula formation 306
of sea urchin blastomeres 306
Gene regulatory networks and skeletogenic mesenchyme
specification 307
Specification of the vegetal cells 310
Sea Urchin Gastrulation 311
Ingression of the skeletogenic mesenchyme 311
Invagination of the archenteron 315
Early Development in Tunicates 318
Cleavage 318
The tunicate fate map 319
Autonomous and conditional specification of tunicate
blastomeres 320
11
Amphibians and Fish 325
Early Amphibian Development 325
Fertilization, Cortical Rotation, and Cleavage 326
Unequal radial holoblastic cleavage 328
The mid-blastula transition: Preparing
for gastrulation 329
Amphibian Gastrulation 329
Epiboly of the prospective ectoderm 330
Vegetal rotation and the invagination
of the bottle cells 331
Involution at the blastopore lip 334
Convergent extension of the dorsal mesoderm 336
Progressive Determination of
the Amphibian Axes 339
Specification of the germ layers 339
The dorsal-ventral and anterior-posterior axes 340
The Work of Hans Spemann and Hilde Mangold:
Primary Embryonic Induction 340
Molecular Mechanisms of Amphibian Axis
Formation 342
How does the organizer form? 343

Functions of the organizer 348
Induction of neural ectoderm and dorsal mesoderm:
BMP inhibitors 348
Conservation of BMP signaling during
dorsal-ventral patterning 351
Regional Specificity of Neural Induction along
the Anterior-Posterior Axis 351
Specifying the Left-Right Axis 355
Early Zebrafish Development 356
Zebrafish Cleavages: Yolking Up the Process
Gastrulation and Formation of the Germ Layers
Progression of epiboly 361
Internalization of the hypoblast 362
The embryonic shield and the neural keel 363
Dorsal-Ventral Axis Formation 364
The fish blastopore lip 365
Teasing apart the powers of Nodal and BMP during axis
determination 365
Left-Right Axis Formation 367
PART IV ● Building with Ectoderm:
The Vertebrate Nervous Systyem and Epidermis
13
Neural Tube Formation and Patterning 401
Transforming the Neural Plate into a Tube:
The Birth of the Central Nervous System
Primary neurulation 404
Secondary neurulation 412
Patterning the Central Nervous System 413
The anterior-posterior axis 413
The dorsal-ventral axis 415
Opposing morphogens 416
All Axes Come Together 419
Contents   xi
12
Birds and Mammals 369
Early Development in Birds 371
Avian Cleavage 372
Gastrulation of the avian embryo 372
Axis specification and the avian “organizer” 377
358
Left-right axis formation 379
361
Early Development in Mammals 380
Mammalian cleavage 380
Trophoblast or ICM? The first decision of the rest of your
life 382
Mammalian gastrulation 383
Mammalian axis formation 388
Twins 394
Coda 396
14
Brain Growth 421
Neuroanatomy of the Developing
403 Central Nervous System 422
The cells of the developing central nervous system 422
Tissues of the developing central nervous system 422
Developmental Mechanisms
Regulating Brain Growth 427
Neural stem cell behaviors during division 427
Neurogenesis: Building from the bottom up
(or from the inside out) 428
Glia as scaffold for the layering of the cerebellum
and neocortex 430
Signaling mechanisms regulating development
of the neocortex 431
Development of the Human Brain 434
Fetal neuronal growth rate after birth 434
Hills raise the horizon for learning 435
Genes for brain growth 437
Changes in transcript quantity 438
Teenage brains: Wired and unchained 438
xii   
Contents

Local and long-range guidance molecules:

15 The street signs of the embryo 470
Repulsion patterns: Ephrins and semaphorins 470
How Did the Axon Cross the Road? 471
Neural Crest Cells and …Netrin 472
Axonal Specificity 441 Slit and Robo 473
The Travels of Retinal Ganglion Axons 475
The Neural Crest 441 Growth of the retinal ganglion axon to
Regionalization of the Neural Crest 443 the optic nerve 476
Growth of the retinal ganglion axon
Neural Crest: Multipotent Stem Cells? 444
through the optic chiasm 476
Specification of Neural Crest Cells 446
Target Selection: “Are We There Yet?” 477
Neural Crest Cell Migration: Epithelial to Chemotactic proteins 477
Mesenchymal and Beyond 447 Target selection by retinal axons:
Delamination 448 “Seeing is believing” 478
The driving force of contact inhibition 450
Synapse Formation 480
Collective migration 451
Migration Pathways of Trunk Neural Crest Cells 452
The ventral pathway 453
The dorsolateral pathway 455 16
Cranial Neural Crest 457
The “Chase and Run” Model 459
Ectodermal Placodes and
An elaborate collaboration of pushes and pulls 459 the Epidermis 485
Neural Crest-Derived Head Skeleton 461
Cranial Placodes: The Senses of Our Heads 486
Cardiac Neural Crest 462 Cranial placode induction 487
Establishing Axonal Pathways Otic-epibranchial development: A shared
in the Nervous System 464 experience 488
The Growth Cone: Driver and Engine Morphogenesis of the vertebrate eye 493
of Axon Pathfinding 465 Formation of the eye field: the beginnings
Rho, Rho, Rho your actin filaments down of the retina 494
the signaling stream 466 The lens-retina induction cascade 495

Axon Guidance 467
The Intrinsic Navigational Programming
of Motor Neurons 467
Cell adhesion: A mechanism to grab the road
The Epidermis and Its Cutaneous Appendages 498
Origin of the epidermis 498
The ectodermal appendages 499
469 Signaling pathways you can sink your teeth into 501
Ectodermal appendage stem cells 502

PART V ● Building with Mesoderm and Endoderm: Organogenesis

17
Paraxial Mesoderm
The Somites and Their Derivatives
Cell Types of the Somite 510
Establishing the Paraxial Mesoderm and
Cell Fates along the Anterior-Posterior Axis 511
Specification of the paraxial mesoderm 511
Spatiotemporal collinearity of Hox genes
determines identity along the trunk 513
507 Somitogenesis 516
Axis elongation: A caudal progenitor zone
and tissue-to-tissue forces 516
How a somite forms: The clock-wavefront model 520

Linking the clock-wavefront to Hox-mediated axial
identity and the end of somitogenesis 526
Sclerotome Development 528
Vertebrae formation 528
Tendon formation: The syndetome 532
Dermomyotome Development 534
Determination of the central dermomyotome
Determination of the myotome 535
18
Intermediate and Lateral Plate Mesoderm
Heart, Blood, and Kidneys 541
Intermediate Mesoderm: The Kidney 542
Specification of the Intermediate Mesoderm:
Pax2, Pax8, and Lim1 544
Reciprocal Interactions of Developing
Kidney Tissues 545
Mechanisms of reciprocal induction 546
Lateral Plate Mesoderm: Heart and
Circulatory System 550
Heart Development 552
A minimalist heart 552
Formation of the heart fields 552
Specification of the cardiogenic mesoderm 554
Migration of the cardiac precursor cells 555
Initial heart cell differentiation 557
Looping of the heart 557
Blood Vessel Formation 559
Vasculogenesis: The initial formation
of blood vessels 559
Angiogenesis: Sprouting of blood vessels
and remodeling of vascular beds 561
Hematopoiesis: Stem Cells and Long-Lived
Progenitor Cells 563
Sites of hematopoiesis 563
The bone marrow HSC niche 565
Coda 567
Contents   xiii
19
Development of the Tetrapod Limb 571
535 Limb Anatomy 572
The Limb Bud 572
Hox Gene Specification of Limb Skeleton Identity 574
From proximal to distal: Hox genes in the limb 574
Determining What Kind of Limb to Form
and Where to Put It 576
Specifying the limb fields 576
Induction of the early limb bud 577
Outgrowth: Generating the Proximal-Distal Axis
of the Limb 582
The apical ectodermal ridge 582
Specifying the limb mesoderm:
Determining the proximal-distal polarity 584
Turing’s model: A reaction-diffusion mechanism
of proximal-distal limb development 587
Specifying the Anterior-Posterior Axis 591
Sonic hedgehog defines a zone of polarizing activity 591
Specifying digit identity by Sonic hedgehog 591
Sonic hedgehog and FGFs: Another positive
feedback loop 594
Hox genes are part of the regulatory network specifying
digit identity 595
Generating the Dorsal-Ventral Axis 599
Cell Death and the Formation of Digits
and Joints 600
Sculpting the autopod 600
Forming the joints 601
Evolution by Altering Limb Signaling Centers 602
20
The Endoderm Tubes and Organs for
Digestion and Respiration 607
The Pharynx 609
The Digestive Tube and Its Derivatives 611
Specification of the gut tissue 612
Accessory organs: The liver, pancreas, and gallbladder 614
The Respiratory Tube 619
Epithelial-mesenchymal interactions and
the biomechanics of branching in the lungs 620
xiv   
Contents
PART VI ● Postembryonic Development
21
Metamorphosis
The Hormonal Reactivation of Development
Amphibian Metamorphosis 626
Morphological changes associated
with amphibian metamorphosis 627
Hormonal control of amphibian metamorphosis 629
Regionally specific developmental programs 631
Metamorphosis in Insects 632
Imaginal discs 633
Hormonal control of insect metamorphosis 636
The molecular biology of 20-hydroxyecdysone
activity 638
Determination of the wing imaginal discs 639
22
Regeneration
The Development of Rebuilding 643
Defining The Problem of Regeneration
Regeneration, a Recapitulation of Embryonic
Development? 645
An Evolutionary Perspective on Regeneration
Regenerative Mechanics 650
Plant Regeneration 650
A totipotent way of regenerating 650
A plant’s meri-aculous healing abilities 652
Whole Body Animal Regeneration 656
Hydra: Stem cell-mediated regeneration, orphallaxis,
and epimorphosis 656
Stem cell-mediated regeneration in flatworms 659
Tissue-Restricted Animal Regeneration 668
Salamanders: Epimorphic limb regeneration 668
Defining the cells of the regeneration blastema 668
Luring the mechanisms of regeneration
from zebrafish organs 673
Regeneration in Mammals 679
Compensatory regeneration in the mammalian liver 679
625 The spiny mouse, at the tipping point between
scar and regeneration 681
23
Development in Health and Disease
Birth Defects, Endocrine Disruptors,
and Cancer 685
The Role of Chance 686
Genetic Errors of Human Development 686
The developmental nature of human syndromes 686
Genetic and phenotypic heterogeneity 687
Teratogenesis: Environmental Assaults
on Animal Development 688
Alcohol as a teratogen 690
Retinoic acid as a teratogen 694
Endocrine Disruptors: The Embryonic Origins
of Adult Disease 695
644
Diethylstilbestrol (DES) 697
Bisphenol A (BPA) 698
Atrazine: Endocrine disruption through
647 hormone synthesis 700
Fracking: A potential new source of
endocrine disruption 701
Transgenerational Inheritance of Developmental
Disorders 702
Cancer as a Disease of Development 703
Development-based therapies for cancer 708
Coda 709
 Contents  xv

PART VII ● Development in Wider Contexts

Mechanisms of Evolutionary Change 742
24 Heterotopy 742
Heterochrony 744
Heterometry 745
Development and the Environment Heterotypy 746
Biotic, Abiotic, and Symbiotic Regulation Developmental Constraints on Evolution 747
of Development 711 Physical constraints 748
Morphogenetic constraints 748
Developmental Plasticity: The Environment as Pleiotropic constraints and redundancy 748
an Agent in Producing Normal Phenotypes 711
Diet-induced polyphenisms 713
Ecological Evolutionary Developmental
Biology 749
Predator-induced polyphenisms 715
Temperature as an environmental agent 716 Plasticity-First Evolution 749
Reaction norms in plants 718 Genetic assimilation in the laboratory 750
Larval settlement 720 Genetic assimilation in natural environments 751
Stress as an agent: The hard life of Selectable Epigenetic Variation 752
spadefoot toads 720
Evolution and Developmental Symbiosis 754
Developmental Symbioses 721 The evolution of multicellularity 755
Developmental symbioses in plants 722 The evolution of placental mammals 756
Mechanisms of developmental symbiosis: Getting the
Coda 756
partners together 724
Developmental symbiosis in the mammalian
intestine 727 Appendix A-1
Coda 731
Glossary G-1

25 Index I-1

Development and Evolution

Developmental Mechanisms of Evolutionary
Change 735

The Developmental Genetic Model of

Evolutionary Change 756
Preconditions for Evolution:
The Developmental Structure of the
Genome 736
Modularity: Divergence through dissociation 736
Molecular parsimony: Gene duplication
and divergence 739
Preface: Thinking Grandly
about Developmental Biology

With biology going into smaller and smaller realms, it is sometimes good to
contemplate the grand scheme of things rather than the details, to “seat thyself
sultanically among the moons of Saturn” (in Herman Melville’s phrase). It is
good, for instance, to get a perspective of developmental biology from outside
the discipline rather than from inside it.

Remembering the Field’s Interdisciplinary Foundations

Developmental biology, history tells us, is an interdisciplinary field that is at the
foundations of biology. Indeed, before the word biology came to be used, the liv-
ing world was characterized as that part of the world that was developing. The
organizers of the first meeting (in 1939) of the Growth Society, which was the
precursor of the Society for Developmental Biology, claimed that development
must be studied by combining the insights of numerous disciplines, including ge-
netics, endocrinology, biochemistry, physiology, embryology, cytology, biophysics,
mathematics, and even philosophy. Developmental biology was to be more than
embryology. It also included stem cells, which were known to generate the adult
blood, and regeneration, which was seen to be the re-activation of developmental
processes and which was critical for healing in vertebrates and for reproduction of
hydra, flatworms, and numerous other invertebrates. The first articles published
in the journal Developmental Biology showcased embryology, regeneration, and
stem cells, and the different ways of studying them.
Throughout this new 12th edition you will see a return to some of these found-
ing ideas of interdisciplinary developmental biology, namely regeneration, mor-
phomechanics, plants, and the genetic control of development.
Indeed, regeneration has historically been a major part of developmental biol-
ogy, for it is a developmental phenomenon that can be readily studied. Experimen-
tal biology was born in the efforts of eighteenth-century naturalists to document
regeneration and to examine how it was possible. The regeneration experiments of
Tremblay (hydras), Réaumur (crustaceans), and Spallanzani (salamanders) set the
standard for experimental biology and for the intelligent discussion of one’s data.
More than two centuries later, we are beginning to find answers to the great
problems of both embryology and regeneration. Indeed, the conclusions of one
support the research of the other. We may soon be able to alter the human body
so as to permit our own limbs, nerves, and organs to regenerate. Severed limbs
could be restored, diseased organs could be removed and regrown, and nerve
cells altered by age, disease, or trauma could once again function normally. The
ethical issues this would exacerbate are only beginning to be appreciated. But if
we are to have such abilities, we first have to understand how regeneration oc-
curs in those species that have this ability. Our new knowledge of the roles that
paracrine factors and physical factors play in embryonic organ formation, plus
recent studies of stem cells and their niches, has propelled what Susan Bryant has
called “a regeneration renaissance.” Since “renaissance” literally means “rebirth,”
and since regeneration can be seen as a return to the embryonic state, the term
is apt in many ways.
xviii   
Preface

Notice that biophysics was also an early part of the mix of developmental biol-
ogy. This area, too, is having a renaissance. The physical connections between
cells, the strength of their bonding, and the tensile strength of the material sub-
strates of the cells are all seen to be critical for normal development. Physical
forces are necessary for sperm-egg binding, gastrulation, heart development,
gut development, the branching of the kidney and lung epithelia, and even the
development of tumors. Physical forces can direct the development of stem cells
toward particular fates, and they can determine which part of the body is left
and which is right. The patella of our kneecap doesn’t form until we put pres-
sure on it by walking. In many cases, physical forces can direct gene expression.
Lev Beloussov, a pioneer in this area, has called this the “morphomechanics of
development.”
Another area that was prominently represented in the early programs of devel-
opmental biology was plant development. Plant development had much in common
with regeneration, as “adult” plants could redevelop entire parts of their bodies.
Whereas in animal biology the study of development diverged from the study
of physiology, that separation was not evident in plant biology. Moreover, while
many animals quickly set aside a germline that was to become the sperm or eggs,
this was not the case in plants. Such comparisons between plants and animals are
now present throughout this text, and they serve to highlight the fundamental
developmental processes that are present across phyla and even kingdoms of life.
But the genes remain the center of focus in developmental biology. And the
more we learn about them, the more interesting and complex these genes be-
come. New advances in “single cell transcriptomics” have given us an amazing
privilege—the ability to look at the gene expression patterns of individual cells
as they develop. An individual’s cells may all have the same genes, but their dif-
ferent positions in the embryo cause different genes to be active in each cell. It’s a
symphony of relationships, each cell providing the context for another. If develop-
ment is the performance, then the genome is the script or score. As anyone who
has gone to concerts knows, different bands perform the same score differently,
and the same band will play the same song differently on two successive nights.
Environment is also critical—hence, the new interest in plasticity and symbiosis
in development.
Developmental biology has also taken on a new role in science. More than
any other biological science, it demonstrates the critical importance of processes
as opposed to entities. In many organisms, the same process can be done by
different molecules. “It’s the song, not the singer,” say Doolittle and Booth, and
we can be thankful that there are redundant pathways in development—if one
pathway fails, another is often able to take over its function. The entity/process
split in developmental biology mirrors the particle/wave dichotomy in physics.
It is a “both, and” situation, rather than an “either/or” situation. In 1908, the
Scottish physiologist J. S. Haldane said, “That a meeting point between biology
and physical science may at some time be found, there is no doubting. But we
may confidently predict that if that meeting-point is found, and one of the two
sciences is swallowed up, that one will not be biology.” Developmental biology
may well solve the longstanding mysteries of physics.

New to the Twelfth Edition

In this current volume, we have attempted to track this amazing fulfillment of
the early promises of developmental biology. To this end, the book has undergone
its own morphogenesis.

Plant development covered throughout

We have now incorporated plant material into the relevant chapters. Instead of
segregating plant developmental biology into a single (and often unassigned)
 Preface   xix

chapter, we have integrated essential plant biology into the chapters on cell speci-
fication, gene regulation, cell communication, gamete production, fertilization,
axis determination, organ formation, and regeneration.

Upgraded and expanded chapter on regeneration

We have also expanded the chapter on regeneration, which we are proud to say
offers a unique summary of the field. It both captures the fascinating problems
of post-embryonic development that regeneration seems to solve and provides
a logical framework for the known mechanisms of regeneration, based on an
organism’s degree of regenerative capacity. We feel that this chapter will be an
excellent place for anyone interested in this area to start.

Updates throughout all chapters

All of the chapters have received important updates, from the introductory chap-
ter’s broader evolutionary perspective to new material on the morphomechanics
of development during Drosophila gastrulation and the formation of mammalian
lungs. Special consideration was also given to the increasing use of whole-ge-
nome, transcriptomic approaches, which are dramatically shaping our under-
standing of cell differentiation.

A new, student-centered approach

From a pedagogical standpoint, it is also good to get an outside perspective of
how students are learning developmental biology—the perspective of the student
experience. For decades, it has been the responsibility of textbooks like ours to be
the most comprehensive sources for the field’s foundational content. Although
this responsibility still remains, the reality is that students are inundated with an
overwhelming myriad of sources vying for their attention. If there was ever a time
a student of developmental biology needed a guidebook to navigate through this
dense and diverse ecosystem of texts, online resources, and infinitely expand-
ing scientific literature, the time is now and the guidebook this new volume of
Developmental Biology.

• Focused and streamlined coverage. Over the years, as new knowledge has
grown, so has our own textbook, which was reaching a size that might
itself trigger student overload and defeat the purposes of engagement
and deep learning. The information bombarding students is not going
away; therefore, they need not only access to the information but also a
clear guide that fosters movement from the essential ideas to the com-
plex mechanisms and finally to inclusive invitations that welcome their
research in this field. We have both reduced and reorganized the content
in each chapter to achieve a clear and supportive lattice so that both the
professor and the student can more easily navigate the increasing vol-
ume and complexity of developmental biology.
• Innovative pedagogy: Empowering students to craft their own learning. The
first material students will encounter in each section of a chapter rep-
resents the most essential content. We have introduced a new element
called “Further Development,” which highlights content we feel repre-
sents some of the more complex ideas in the field. In addition, students
will also come across invitations to view some Further Developments
online. These online topics represent fantastic opportunities for students
to further develop their understanding of developmental biology along
paths of their own interest—paths of investigation that professors can
have confidence match the standards of quality seen throughout the
textbook (unlike some other online sources). The special in-text fea-
tures of previous editions—Dev Tutorials, Developing Questions, Next
Step Investigations, and citations throughout—are still in place to play
xx   
Preface

important roles in empowering students to take that final leap to engage

with the developmental biology literature. To better support students’
use of the research literature, we now include a new Appendix focused
on how to find and analyze research articles in developmental biology.

Thanks to this new organization of content, professors and students will now
be in complete control of what level of material may be most appropriate. We are
proud to introduce Developmental Biology 12e, as it still provides direct access to
all levels of the content but without diluting its quality and the overall learning
experience.

Acknowledgments
First, the two authors gratefully acknowledge their mutual respect for one an-
other and for the enjoyment of each other’s work. Michael wants the community
to know that Scott has been most accepting and welcoming to new ideas and
that his enthusiasm for producing the best product has not wavered any day
of any edition. Scott wants the community to know that he is thrilled with the
new ideas that Michael has brought to the book and that Michael’s commitment
to undergraduate education is second to none.
Second, we are thrilled to acknowledge the importance of Mary Stott Tyler to
this book. The winner of the Viktor Hamburger Education Award and the author
of Fly Cycle, Differential Expressions, The Developmental Biology Vade Mecum, and
Inquiry Biology, Mary has been a mixture of author, editor, and curator of contents
for this 12th edition, helping us decide “what to leave in/what to leave out.” As we
added plant studies to the book and had to remove other studies, Mary’s insight
and vision for the finished book was essential.
If science is like a balloon expanding into the unknown—and the larger the
balloon, the more points in contact with the unknown—then developmental
biology has contacted an astounding number of unknowns. The accuracy and
coverage of the 12th edition owes much to the work of the many expert reviewers
who took the time to provide respectful formal and informal feedback throughout
the process (see list). The organization of these reviews was consistently executed
by Lauren Cahillane, Nina Rodriguez-Marty and Katie Tunkavige—thank you
for making this important part possible. This 12th edition is particularly unique
as it marks the new incorporation of plant developmental biology. There were
numerous reviewers who offered their expertise in select chapters, thank you to
all. Special thanks, however, go to Anna Edlund and Marta Laskowski for their
reviews of the plant content. They were very patient with us, and any misunder-
standings are those of the authors.
This edition also marks a dramatic change to the publishing of Developmental
Biology. With the retirement of Andy Sinauer, Sinauer Associates has become an
imprint of Oxford University Press. Our book overlaps these two periods, and has
seen the change of managers, art directors, and our long-time editor. We thank
both Sinauer Associates and Oxford University Press for their great efforts in
sustaining the book during this period of metamorphosis. We wish to especially
thank Dean Scudder for taking on the managerial tasks and allowing us to work
on new models of science education during this transition. Moreover, half-way
through production of this edition, Jason Noe of Oxford became our overseeing
editor. Such a transition and short timeline for production might rattle the best of
editors, but Jason helped to establish the best adaptable plans to keep things on
track. Sincere thanks for your efforts, Jason. Meanwhile, in the house of Sinauer,
production editors Laura Green and Kathaleen Emerson shared their expertise
and their truly collaborative insights, offering us respectful considerations during
key times that we will not forget. Thank you Laura for also sharing with us your
most valuable plant background throughout the editorial process.
 Preface   xxi

The success of this and each edition equally rests on the quality of the book’s
design and look, for which we sincerely appreciate the wonderful work Sinauer’s
art, media, and overall production team have done. The media team was headed by
Suzanne Carter and supported by the creative drive of Peter Lacey. Sincere thanks
to you both. Further thanks to the entire group at Dragonfly Media, who continue
to do a great job taking care to represent many of Michael’s original drawings
with supreme accuracy. We’d also like to thank Joan Gemme, Beth Roberge, and
Annette Rapier for their excellent design, layout, and production of this edition.
One of the long-loved hallmarks of Developmental Biology has been the incor-
poration of actual data and images that represent the science. Special thanks to
the permissions team, Mark Siddall, Tracy Marton, and Michele Beckta for their
non-stop efforts in securing the rights to these essential pieces of the book. But
of course, a new book can only reach the hands of the students with the help of
a robust and strategic sales team. Many thanks to Susan McGlew and to all the
salespersons at Oxford now helping to support this textbook.
Lastly, it needs to be acknowledged that while Scott is blissfully retired,
Michael is still working his tail off doing teaching, research, committee assign-
ments, and so forth, in addition to his strong family commitments. He would
not be able to provide the time and energy to this textbook if he did not have
the support of his own institution and students. Thank you, Smith College, for
continuing to allow Michael to produce and disseminate his Web Conferences,
Developmental Documentaries, and the Dev Tutorials freely to the community.
Most sincere thanks to Michael’s research students, who had to endure their
principle investigator being too engrossed in all things development all the time!
Know that your patience, support, and insights surely made this book possible.

­— M.J.F.B.
—S.F.G.
May 24, 2019
Reviewers of the Twelfth Edition
Anna Allen, Howard University
William Anderson, Harvard University
Nicola Barber, University of Oregon
Madelaine Bartlett, University of Massachusetts, Amherst
Marianne Bronner, California Institute of Technology
Timothy Brush, University of Texas, Rio Grande Valley
Blanche Capel, Duke University
Jacqueline Connour, Ohio Northern University
D. Cornelison, University of Missouri, Columbia
Dr. Angus Davidson, The University of Nottingham
Anna Edlund, Bethany College
Elizabeth D. Eldon, California State University, Long Beach
Deborah Marie Garrity, Colorado State University
Bob Goldstein, University of North Carolina
Eric Guisbert, Florida Institute of Technology
Jeff Hardin, University of Wisconsin, Madison
Richard Harland, University of California Berkeley
Marcus Heisler, The University of Sydney
Arnold G Hyndman, Rutgers University
Zhi-Chun Lai, Pennsylvania State University
Michael Lehmann, University of Arkansas
Michael Levin, Tufts University
Yuanyuan Rose Li, University of Alabama at Birmingham
Barbara Mania-Farnell, Purdue University Northwest
Adam C. Martin, Massachusetts Institute of Technology
David Matus, Stony Brook University
Roberto Mayor, University College London
Dave McClay, Duke University
Claus Nielsen, University of Copenhagen
Fred Nijhout, Duke University
Lee Niswander, University of Colorado, Boulder
Julia Oxford, Boise State University
Mark Peifer, University of North Carolina
Isabelle Peter, California Institute of Technology
Ann Rougvie, University of Minnesota
Sabrina Sabatini, Sapienza University of Rome
Thomas F. Schilling, University of California, Irvine
Nick Sokol, Indiana University
Richard Paul Sorrentino, Auburn University
Ana Soto, Tufts University
David Stachura, California State University, Chico
Claudio Stern, University College London
Andrea Streit, King’s College London
Keiko Sugimoto, RIKEN
Jonathan Sylvester, Georgia State University
Daniel E Wagner, Harvard Medical School
Zhu Wang, University of California, Santa Cruz
Paul M. Wassarman, Icahn School of Medicine at Mount Sinai
Daniel Weinstein, Queens College, CUNY
Jessica LaMae Whited, Harvard University
Jeanne Wilson-Rawls, Arizona State University
Colleen Winters, Towson University
Tracy Young-Pearse, Harvard Medical School
Media and Supplements
to accompany Developmental Biology, Twelfth Edition
For the Student
Companion Website
devbio.com
Significantly enhanced for the Twelfth Edition, and refer-
enced throughout the textbook, the Developmental Biology
Companion Website provides students with a range of en-
gaging resources to help them learn the material presented
in the textbook. The companion site is available free of
charge and includes resources in the following categories:
• Dev Tutorials: Professionally produced video
tutorials, presented by the textbook’s authors,
reinforce key concepts.
• Watch Development: Putting concepts into
action, these informative videos show real-life
developmental biology processes.
• Further Development: These extensive topics
provide more information for advanced students,
historical, philosophical, and ethical perspectives
on issues in developmental biology, and links to
additional online resources.
• Scientists Speak: In these lectures and question-
and-answer interviews, developmental biology
topics are explored by leading experts in the field.
• Flashcards: Per-chapter flashcard sets help stu-
dents learn and review the many new terms and
definitions introduced in the textbook.
• Literature Cited: Full citations are provided for
all of the literature cited in the textbook (most
linked to their PubMed citations).
• Research Guide: This illustrated and annotated
guide helps students find and comprehend
research articles in developmental biology.
For the Instructor
(Available to qualified adopters)
Instructor’s Resource Library
The Developmental Biology, Twelfth Edition Instructor’s
Resource Library includes the following resources:
• Case Studies in Dev Bio: This collection of case
study problems provides instructors with ready-
to-use in-class active learning exercises. The case
studies foster deep learning in developmental
biology by providing students an opportunity
to apply course content to the critical analysis of
data, to generate hypotheses, and to solve novel
problems in the field. Each case study includes a
PowerPoint presentation and a student handout
with accompanying questions.
• Developing Questions: Thought-provoking
questions, many with answers, references, and
recommendations for further reading, are pro-
vided so that you and your students can explore
questions that are posed throughout each chapter.
• Textbook Figures & Tables: All of the textbook’s
figures, photos, and tables are provided both in
JPEG and PowerPoint formats. All images have
been optimized for excellent legibility when pro-
jected in the classroom.
Value Options
eBook
(ISBN 978-1-60535-823-9)
Developmental Biology, Twelfth Edition is available as
an eBook, via several different eBook providers, including
RedShelf and VitalSource. Please visit the Oxford Univer-
sity Press website at oup.com/ushe for more information.
Looseleaf Textbook
(ISBN 978-1-60535-824-6)
Developmental Biology, Twelfth Edition is also available in
a three-hole punched, looseleaf format. Students can take
just the sections they need to class and can easily integrate
instructor material with the text.
Another random document with
no related content on Scribd:
advantage in the chorus that there was no doubt about its success.
They were importuned upon this revelation of their talent to sing a
solo apiece. They contrived to evade this penalty on the plea that
they had never sung in public before, although Goose declared that
Muffin had sung by herself twice in Slocum Magna parish church
with great distinction.
“But that wasn’t in public,” said Muffin, staunchly. “Besides, it was
after dearest papa had preached his sermon.”
“I am afraid, my dear Miss Muffin,” said Cheriton, “that the point is
too subtle for the lay intelligence.”
Although Muffin and Jim Lascelles were absolved from singing solos,
they were unable wholly to evade the penalty incurred by the
revelation of their gifts. They were haled to the piano to sing a duet
from H.M.S. Pinafore; and made such a hopeless mess of the
performance that Jim’s mother, to whom the accompaniment was
intrusted, took the extreme course of closing the piano in the middle
of it and retiring in dudgeon.
A display of thought-reading concluded the proceedings. The Vicar’s
wife was a clairvoyante, noted for miles around. Cheriton also
confessed to powers in this occult science. The Vicar’s wife was only
permitted to perform one feat, because the Vicar declared that if she
attempted more than one in an evening it excited her so much that
she never slept all night. The task allotted to her was that she should
take the ribbon from Ponto’s neck and tie it around Goose’s finger.
The feat was performed with such exemplary ease that Muffin felt
sure that she could do something. Her task was the elementary one
of giving Miss Burden a kiss. Instead of doing this, however, she
hugged Aunt Caroline. In the opinion, however, of those best
acquainted with these mysteries, she was held to be so nearly right
that her reputation was established forthwith.
“Isn’t it wonderful?” said Goose, with dilated eyes. “I shall write to
dearest papa about it. At the next entertainment in Slocum Magna
parish-room Muffin will have to do something.”
“I think,” said Jim’s mother, “her powers as a clairvoyante are
superior to her powers as a cantatrice.”
Muffin was showing a desire to give a further display of her newly
discovered talent, when Aunt Caroline said it was half-past ten, and
that Araminta and Elizabeth must retire.
After saluting Aunt Caroline in a very dutiful manner they obeyed this
edict with most admirable docility. It proved a signal for the general
dispersal of the company. There is reason to believe that Aunt
Caroline intended that it should.
No sooner were the Vicar and his wife and Jim Lascelles and his
mother abroad in the rapt summer stillness, and they were picking
their way through the tomblike darkness of the wood towards Pen-y-
Gros hamlet, than the inmates of the castle sat down to the green
table. Caroline Crewkerne yawned vigorously. But her opponents did
well not to misinterpret that action, because this old woman was
never known to sit down to cards without proving herself to be more
than usually wide-awake.
“Caroline,” said her oldest friend, “this is certainly one of the whitest
days in all my recollection of you. I can’t say positively that you were
genial, but I feel that I am entitled to affirm that you got through the
evening without insulting anybody.”
“The middle classes are so tiresome,” said Caroline, cutting for the
deal and winning it easily.
“The middle classes are almost extinct as a genus,” said Cheriton.
“They have assimilated culture so rapidly since that fellow Arnold
wrote to them upon the subject that nowadays they are almost as
extinct as the dodo.”
“Pshaw!” said Caroline, carefully sorting a hand that contained four
aces and three kings. “It is only skin deep. Don’t be a coxcomb,
Cheriton. I declare no trumps.”
“I shall not double,” said Cheriton, who found himself in possession
of a “Yarborough.”
In a very short space of time, Cheriton and Miss Burden had suffered
the indignity of the “grand slam.”
“Well played, partner,” said George, as soon as he woke up.
There can be really no question at all that few persons could have
played their cards better than Caroline Crewkerne, when that old
woman found herself with a good hand. And few persons found
themselves oftener in that enviable position than did she. Certainly
this evening she surpassed herself. It is true that the cards came her
way in the most surprising fashion. But she utilized them to the full;
and further, she took advantage of the mistakes of her principal
adversary.
It was not often that Cheriton was guilty of flagrant errors, but on this
occasion he certainly held bad cards, and to these he added
unmistakably inferior play. He forgot important cards constantly; and
twice at a critical moment he revoked. Caroline was in the highest
glee. Everything went right for her; and the sum she won from
Cheriton it would not be wise or right to divulge, lest it shock the less
affluent among our readers. It was not really enough “to endow a
hospital for the incurably insane,” as Cheriton declared it was, but it
certainly enabled the lucky Caroline to contemplate the purchase of
a few of those Westralians which she had coveted for some time
past.
Happily neither Miss Burden nor George Betterton could afford to
play for money; the former because her salary of forty pounds per
annum was her only means of subsistence; the latter because his
high rank rendered it necessary that in all respects his life should be
a pattern to his admiring countrymen. We have no desire to lower a
very worthy man in the public estimation, but this desire for
respectability did not prevent his losing continually at piquet to
Caroline Crewkerne. But then piquet is not like bridge. The one is old
and of good report; the other is new and plutocratic.
A little after midnight George Betterton retired in earnest to his
virtuous repose, while Miss Burden followed his example. And no
sooner had the hostess and her old friend the field to themselves
than they reverted to the topic of the previous night. The matter had
been left in an interesting stage. Cheriton felt it to be a hopeful one.
He was sure that he had no serious rival to contend against, for
George with all his flourishes was sure to end by marrying Priscilla.
The Georges of this world invariably marry the Priscillas.
“I am willing to tie three thousand a year upon the creature,” said
Cheriton. His tone was not exactly that of an auctioneer, although his
standard of wisdom rendered it necessary that he should always suit
his discourse to his company. “Upon the condition, my dear Caroline,
that you tie an equal sum upon her. And there is also a living in my
gift worth eleven hundred a year which is likely to be vacant.”
So much for the terms. Caroline Crewkerne pondered them well.
She was a shrewd, covetous, hard-headed, hard-hearted old
woman. But if she took a thing in hand she carried it through. And
she had determined to do something for her dead and disgraced
sister’s portionless daughter. Up to a point she was able to plume
herself upon the success of the negotiations. What she did not like
was the sacrifice of some of her own money. It would not make the
least difference to her. She had more already than she knew what to
do with, but to part with her substance always hurt her.
“We will say fifteen hundred, Cheriton, and call it settled,” said
Caroline with the air of a money-lender.
Her old friend frankly enjoyed the situation. He knew where the shoe
pinched as well as she did. Her craft and her avarice reminded him
of Balzac’s novels.
“If you say fifteen hundred, my dear Caroline,” said her old friend, “I
must say fifteen hundred too.”
Caroline pondered again. Cheriton was not a good life, and nearly
everything was entailed.
“Three thousand a year in perpetuity?” said Caroline, harshly.
“Ye-es,” said Cheriton. “Dooced liberal, I think, for a poor parson’s
daughter.”
Caroline bristled. She looked not only prickly but venomous.
“Don’t forget, Cheriton,” she said truculently, “that the creature is a
Wargrave.”
“An effete strain, there is reason to fear,” said Cheriton with perfect
composure.
The head-dress performed surprising feats. Cheriton fell to
considerations of how far it might be safe to bait the old lioness. No
sport is worth much without there is a spice of danger in it. He
enjoyed the play none the less because he was so sensible of its
peril. Caroline Crewkerne was not a person to be baited with
impunity.
However, in spite of the head-dress and the gleams of red that
flashed from the ruthless orbs beneath it, he was able to assume an
aspect of excellent indifference. The finished duplicity may not have
deceived his old friend or it may have done so. At least the old
lioness grew more couchant in her aspect. But the mouth was as
resolute in its sarcasm as ever.
“Well, Caroline,” said Cheriton, amiably, “let us settle the thing one
way or the other. It is becoming tedious.”
Perhaps Caroline thought so too. Or perhaps she thought she had
made a reasonably good bargain, all things considered, and that she
was not likely to do better. For there came a further accession of
scorn to the grim old countenance, and for a moment the head-dress
ceased its immodest gyrations.
“Take the girl and be damned,” said Caroline Crewkerne.
Cheriton bowed with ironical politeness. He had got his way, not of
course that there was anything surprising in that. He had had it so
often. Still there was a certain satisfaction in it, for it always seems a
part of the essential fitness of things that one should get one’s way,
no matter how much one is accustomed to getting it. He was also a
little inclined to plume himself, as was too often the case with him, on
his diplomacy. It was really an achievement to screw a cool three
thousand a year out of the most avaricious old woman in England.
Yet it may have been that he had only inserted that clause into the
negotiations to give them a further spice. It had enabled him to pose
as the prophet of justice, liberality, and other delectable things. He
had never cared greatly about money, but that was no reason why
he should not bait those who did care greatly about it when he was
in need of a little private relaxation.
Cheriton went to bed and slept the sleep of the just. By the exercise
of his talents he had got a charming countess on liberal terms. How
the young fellows would envy him! His affectation of youth would
now lose its point. Upon the day he married his young goddess he
would resume his natural age, which was sixty-five. In his mind’s eye
he could see himself walking down the aisle on the happy occasion
with all the gravity of a pillar of the Government, of one eminent in
council, looking if anything rather more than his years in order to
score off the rising generation.
“He is so old, my dear!” he could hear the buzz of tongues. Yes, so
old; what had happened to Youth and its vaunted pretensions?
Caroline Crewkerne went to bed, and she slept the sleep of the just
also. All the same there is really no reason why she should have
done so. For there was precious little justice in that old woman. She
was well satisfied that she had won at cards, but in the matter of her
niece she had a very decided feeling that that man Cheriton had
overreached her. The clause of the three thousand pounds per
annum took a good deal of the gilt off the gingerbread. Without that
clause there would have been a certain amount of gilt upon it.
Cheriton, for all his coxcombry, was a pretty considerable parti, at
whom the arrows of the worldly had been aimed for two generations.
But in Caroline’s own phrase, “Cheriton was no fool.” In spite of his
vanity and his fribbling he knew his way about the world. He was a
cool hand. He marked his quarry and pursued it at his leisure, in his
own impersonal and peculiar way, and never once had he been
caught napping. Great would be the applause and the merriment
when it became bruited about that this astute bird had actually been
limed by the old fowler of Hill Street. And after all nobody need know
about that three thousand pounds per annum.
Therefore both parties to this transaction slept the sleep of the just,
and next morning had breakfast in their rooms. At half-past five a.m.
the unconscious object of their negotiations was haled out of bed by
her sister Muffin. And as the descent to the floor did not arouse her,
she was beaten about the head with a pillow until that object had
been attained. They spent incomparable hours among the dew on
the slopes of Gwydr and his brethren. Jim Lascelles was with them.
He piloted them among the rocks, and was of course prepared to
save their lives if necessary.
These were indeed golden and enchanted hours. For all her
slowness of speech and action the Goose Girl had a certain
animation and inward fire when in her true Slocum Magna form. Little
of it had been seen in Hill Street, for amid that rather dismal splendor
she was a bird in a cage. But now with the freedom of the mountains
conferred upon her, with Jim upon one hand and Muffin upon the
other, existence was a carol. The old glories of the Red House at
Widdiford were revived.
These joys continued during a number of glorious and golden days.
Cheriton, secure in his prize, was in no hurry to impale his butterfly.
She was a charming picture, and he would claim her at his leisure. In
the meantime let her garner up a store of health and vigor upon the
mountains in the society of her peers. For, truth to tell, the
bridegroom-elect was apt to get fatigued rather easily, and it was
really more satisfying to share a red umbrella with an intellectual
equal and to discuss the French writers beside the lake.
Therefore, with that humane wisdom which distinguished him above
other men, Cheriton was content that each of them should continue
in their paradise as long as it could possibly endure. Things were
going very well as they were. Why disturb them? The prize was
secure. Caroline Crewkerne had given her sanction and had written
to her lawyer upon the subject. There was really no more to be said.
Why imperil the perfect harmony of the passing hour? All in good
season; when there were no mountains, no lakes, no cloudless
August skies, no red umbrellas, no green frocks, no singularly
companionable, cultivated, and agreeable students of the best
French literature, would be the time to speak of love.
Yes, Cheriton was a cool hand. Indeed, so much so that Caroline
Crewkerne was a little inclined to doubt his bona fides.
“I have not seen the creature in tears yet,” said she three days after
that memorable night in which the compact was made.
“Do not let us commit the indiscretion, my dear Caroline,” said the
happy wooer, in his most musical manner, “of acting prematurely. I
have always been a believer in laissez faire. If things are going
obviously right, why disturb them? The creature rejoices like a lark in
her youth, her companions, and her mountains. I am too old for
mountains myself. But do not let us curtail her happiness by a single
hour. And, upon my word, she seems to grow more glorious every
time I look at her.”
“Humph!” said Caroline Crewkerne.
She was too wise to say anything else.
“Let us do nothing, my dear Caroline,” said the happy wooer, “to
impede the spontaneous acquisition of health, vigor, gayety, and
flowerlike simplicity. Upon my word, the bracing climate of the Welsh
mountains has given her a fire and a gladness and natural
spontaneity which I do not think even Borrow himself could wholly
account for. It does one good to sit apart and see it grow.”
“Cheriton,” said Caroline Crewkerne, “if I had not the best of reasons
to know the contrary I should think you were a fool.”
“I am very happy to be one just now,” said he, “in the cause of
youth.”
“You were always a coxcomb,” said his unsparing critic, “and I quite
expect that one of these days you will have to pay a price for it. In
my opinion it is quite time the creature began to shed a few tears.”
“No, no, Caroline. Let us have the common humanity to give her the
undiluted joy of her mountains as long as we can.”
Caroline shook her worldly wise old head. She grew very thoughtful
indeed. There was the question of the red umbrella. But she did not
alarm herself. Cheriton had played that game so often.
The days passed merrily. It was a perfect time, with hardly more than
the suspicion of a cloud about the noble head of Gwydr. And as the
waters of Lake Dwygy preserved their seductive and delicious
coolness it is not to be wondered at that the picture of the naiad
made great progress.
There was no doubt about the wonderful increase of power that had
come to Jim Lascelles. Having given his days to the painting of the
Goose Girl and his nights to thoughts of her, this expenditure of spirit
was now manifesting itself in his brush. The naiad bade fair to be a
brilliantly poetic composition, whose color had that harmonious
daring that had given Monsieur Gillet an European fame. The frank
treatment of the naiad’s blue eyes and yellow hair, which had made
the portrait of her sister so wonderful, were here adjusted to the
majestic scheme of Dwygy’s blue waters, and Gwydr’s brown slopes
crowned with a golden haze, with here and there a black patch of the
woods about Pen-y-Gros. Cheriton, who among his other
recommendations was a trustee of the National Gallery, ministered
to the pride of the painter’s mother by his outspoken praise of what
he considered to be a signal work of art.
The August sunshine, however, cannot last for ever. And at last, as
Muffin’s second triumphant fortnight was nearing its close, the clouds
gathered about Gwydr and his brethren, and the woods of Pen-y-
Gros were drenched with a sopping mist. This presently turned to a
downpour of rain which lasted a day and a night, and in that period
something happened.
 CHAPTER XXVIII
A THUNDERBOLT

WHILE the rain was beating with monotonous persistence upon the
oriel windows of Pen-y-Gros Castle, Araminta was summoned to
Aunt Caroline’s boudoir. So little did that artless being suspect
calamity that she obeyed the summons joyfully, because she felt
convinced that Aunt Caroline was to confer with her as to whether
Muffin would like to stay still longer. But it proved to be something
else.
Aunt Caroline was looking very bleak and formidable, and Lord
Cheriton, who was present also, had never seemed so much like a
parent, so benevolently unbending was his manner.
“Girl,” said Aunt Caroline—she very seldom addressed Araminta in
any other style than “Girl”—“sit there and try not to behave foolishly. I
am going to speak about your future.”
So little was Araminta preoccupied with things in general that she
hardly knew that she had such a thing as a future. However, with her
usual docility, she sat upon the chair that Aunt Caroline had
indicated, and proceeded to give her best attention to her august
relation.
“I will be brief,” said Aunt Caroline, with an extremely businesslike
air. “My old friend Lord Cheriton has been good enough to take an
interest in you, and if you are a good girl he will marry you. You have
no objection, I presume?”
It was clear by Aunt Caroline’s tone that she merely asked the last
question as a matter of form. But that brisk old worldling went a little
too quickly for her niece Araminta, who was really a very slow-witted
creature. Some little time had to pass before she could accept the
purport of Aunt Caroline’s announcement. And when at last she was
able to do so it literally took away her breath.
Aunt Caroline allowed the creature quite thirty seconds in which to
reply. No reply being forthcoming in that space of time, she
proceeded to address her as though she were a prisoner at the bar.
“Well, girl,” said Aunt Caroline, “what have you to say?”
Araminta had nothing to say apparently. But from the uppermost
forehead to the depths of the neck, a slowly deepening wave of
scarlet was spreading over the whole surface of her frank and vividly
colored countenance.
“Humph!” said Aunt Caroline; “no objection apparently.” She then
addressed a third person very succinctly. “Cheriton,” said she, “I
congratulate you. You are not everybody’s choice, and I must
confess to some surprise that no objection has been urged. That is
the Wargrave in her, I dare say. The Wargraves have always known
how to accept the inevitable. They have often gone to the scaffold
rather than make a pother.”
“Family pride again, my dear Caroline,” said Cheriton, in a voice of
honey. “Still, in the circumstances, perhaps a slight display of it is
pardonable. History is not my strong point, but I seem to remember
that between the age of Edward VI. and the age of Victoria the
Wargraves went oftener to the scaffold than anywhere else. To a
layman that always appears to be one of the baffling points about the
pride of old families. If we go back far enough we generally find that
a lawyer who was too astute to be honest established their fortunes;
or a fellow who managed to cheat the troops in Flanders of their food
and clothing.”
“Don’t be a coxcomb, Cheriton,” said Caroline, sharply. “Remember
my niece. I shall expect you to be good to her. Fortunately for herself
she has no brains, but she eats well and sleeps well, she is quite
healthy in every respect, and her disposition is affectionate.”
“Our dear Miss Goose is perfectly charming,” said Cheriton, ogling
Miss Perry, who by this time was trembling violently, and who sat in
solemn scarlet consternation. “I am the proudest man in England.”
Caroline Crewkerne raised a finger.
“You have said enough, Cheriton,” said she. “I have my own opinion
about the transaction, but I am inclined to think the creature might
have done worse. You can go now, girl. Don’t mention this matter to
your sister until you have my permission to do so.”
Miss Perry rose with her usual docility, but in her countenance was
an ever-deepening scarlet. She moved slowly and heavily to the
door of the boudoir without speaking a word, either to her aunt or to
Lord Cheriton. Her hand was already upon the door when she turned
round and faced the former. The blue eyes were full of dismay.
“If you please, Aunt Caroline,” she drawled in her ridiculous manner,
“I don’t quite think I can marry Lord Cheriton.”
The old woman sat up in her chair in the manner of a Lord Chief
Justice who has been confronted with a flagrant contempt of court.
“What do you mean, girl?” said she. “You don’t quite think you can
marry Lord Cheriton. Explain your meaning.”
In the most favorable circumstances it was never very easy for Miss
Perry to explain her meaning. In these she seemed to find
considerable difficulty in doing so. Aunt Caroline gave her exactly
thirty seconds, but Miss Perry required longer than that.
“Speak, girl,” said Aunt Caroline. “Are you dumb?”
Miss Perry was not dumb, but speech had never been so tardy.
“Girl, will you have the goodness to explain,” said the old lady, “why
you are not quite able to marry Lord Cheriton?”
At last Miss Perry was able to furnish the required explanation.
“If you please, Aunt Caroline,” she drawled ridiculously, “I have p-r-r-
romised to marry Jim.”
The old lady’s ebony walking-stick fell to the ground so peremptorily
that Ponto was disturbed in his slumbers.
“Jim!” said Aunt Caroline. “Who, pray, is Jim?”
“Jim Lascelles,” said Miss Perry.
“I presume you mean the painting man,” said Aunt Caroline.
“Yes,” said Miss Perry.
There was a pause in which Cheriton and his old friend looked at
one another long and particularly.
“Hand me my stick, girl,” said Aunt Caroline.
Miss Perry did as she was desired. Her manner of doing it seemed
to imply that she expected to receive physical correction.
“Sit down, girl,” said Aunt Caroline.
Miss Perry resumed her chair, doubtless with an emotion of
thankfulness upon her narrow escape.
“I could not have believed it to be possible,” said Aunt Caroline,
speaking very slowly, “that a Wargrave could have been so
imprudent, so ungrateful, so entirely lacking in self-respect.”
This indictment was delivered in the most deliberate and crushing
manner; but a good deal of the effect was marred because Cheriton
laughed outright in the middle of it. Aunt Caroline, however,
presented a haughty indifference to the behavior of the husband-
elect, who, of course, was not himself a Wargrave, and whose
behavior in this crisis showed that fact clearly.
“Are you mad, girl?” said the old lady. “Answer me.”
“Jim is awfully nice,” drawled Miss Perry.
The ebony walking-stick and the head-dress performed a concerted
piece together which filled Ponto with consternation.
“The creature must be a natural.”
Miss Perry grew bolder, however, as the clear conviction that she
was pledged to Jim Lascelles took a firmer hold upon her.
“We shall not marry just yet, don’t you know,” said Miss Perry, with
the air of one who imparts valuable information. “But Jim is going to
get rich so that he can buy back the Red House at Widdiford, and
then we are going to live in it, and it will be too sweet.”
Aunt Caroline having grown incoherent with legitimate anger it
devolved upon Cheriton to say something.
“Capital!” said he, in a most benevolent manner.
This expression of opinion helped Caroline Crewkerne through her
crisis.
“You inconceivably foolish girl,” said she. “Have you no sense of
decency?”
“Muffin has p-r-r-romised to wear her mauve at the wedding,”
drawled Miss Perry.
Had not the husband-elect blown his nose very vigorously there is
reason to fear that he would again have been guilty of conduct unlike
that of a Wargrave.
“Silence, girl!” said Aunt Caroline. “Don’t speak another word until
you have permission. This comes of crossing the breed. Now listen
to me. The sooner you remove the man Lascelles from that
inconceivably foolish and demoralized head of yours the better it will
be for you. Where is your self-respect? Where is your sense of
decency?”
“Muffin——” said Miss Perry, but she got no farther because an
imperious finger stayed her.
“Don’t speak,” said Aunt Caroline. “Simply listen. Dismiss the man
Lascelles from your mind, and try to remember who you are, and
where you are, and what you are saying. My old friend Lord Cheriton
desires to marry you. Understand that clearly. And he has my
permission to do so. Understand that clearly also. Now you may say
something.”
Miss Perry took advantage of this gracious permission to turn to Lord
Cheriton with a charmingly friendly smile upon her scarlet
countenance.
“It is so dear of you, Lord Cheriton,” she said, “and if I were not going
to marry Jim I would marry you. Perhaps Muffin——”
Aunt Caroline affronted the nerves of Ponto by rapping sharply with
her stick upon the floor.
“You have said sufficient,” said she. “Dismiss the man Lascelles from
your mind once and for all. You are going to marry Lord Cheriton. Is
that quite clear?”
Apparently this was not quite so clear to Miss Perry as it was to Aunt
Caroline. For that Featherbrain opened her eyes so widely that they
seemed to acquire the color of violets, and a look of sheer perplexity
settled upon her frank countenance.
“But if you don’t mind, dearest Aunt Caroline,” said she, “I p-r-r-
romised to marry Jim.”
Aunt Caroline began to storm.
“Is the girl a dolt!” she cried. “Has she no brains at all! Girl, have the
goodness to listen once more. Your father, your brothers, and your
sisters are all poor as mice, are they not?”
“Yes, dearest Aunt Caroline,” said Miss Perry, quite simply.
“Very good. Now heed this carefully. By the terms of your marriage
settlement, which I may say I have been able to arrange not without
difficulty, you will become a countess with six thousand a year in
your own right, with a house to live in, and your father or one of your
brothers will have the reversion of a living worth eleven hundred a
year which is in Lord Cheriton’s gift. Now have you the intelligence to
comprehend all that I have said to you?”
Apparently Miss Perry had. Doubtless her understanding was a
slow-moving and cumbrous mechanism which generally found
infinite difficulty in assimilating the most obvious facts; but it was very
difficult for the most obtuse person to misunderstand Caroline
Crewkerne. Slowly but surely her hard lucidity percolated to the
recesses of Miss Perry’s mind; and just as slowly and as surely as it
did, large solemn tears welled into the eyes that had deepened to
the color of violets. They rolled in ridiculous procession down the
crimson cheeks.
Neither Caroline Crewkerne nor Cheriton was affected easily, but
there was something in the solemn slow-drawn emotion of Miss
Perry that imposed silence upon them. The silence that ensued was
uncomfortable and by tacit consent it was left to Miss Perry herself to
terminate it.
“It is so dear of you both,” she said, “to be so good to me. I shall
write to dearest papa about you, but I p-r-r-romised Jim.”
Aunt Caroline snorted.
“And what do you suppose your father will say to you, you
simpleton,” said she, “when he learns what you have done? Now
take my advice. Send the man Lascelles to me. I will deal with him.
And then you must prepare to marry Lord Cheriton some time in
October.”
But Miss Perry sat the picture of woe. It is true that in the opinion of
Cheriton she sat a perfectly enchanting picture of it; yet at the same
time it gave him no particular pleasure to observe that the absurd
creature was shedding real tears, tears which somehow seemed
almost majestic in their simple sincerity.
Miss Perry was dismissed with strict instructions not to mention the
subject to anyone.
“What a creature!” said Caroline Crewkerne, when the door had
closed upon her niece.
She contented herself with that expression. As for Cheriton, he gave
an amused shrug and said nothing. For all his nonchalance perhaps
he could not help feeling that he had been tempting Providence. Yet
so ingrained was his habit of cynicism that it may not have occurred
to him that he had anything to fear from Jim Lascelles. The young
fellow had not a shilling in the world; he had a good head on his
shoulders; and he had been brought up properly. That in such
circumstances he should have taken the unpardonable liberty of
offering to marry Caroline Crewkerne’s niece was totally at variance
with his knowledge of the world, and of human nature as he
understood it.
Caroline Crewkerne was the first to speak.
“Cheriton,” said she, “we are both of us old enough to know better. In
the first place, you ought not to have brought that man to Hill Street;
and in the second, I ought not to have allowed him to enter the
house. However, the mischief is done. We must now take steps to
repair it.”
“I shall be interested, my dear Caroline,” said Cheriton, in his most
agreeable manner, “to learn what the steps are you propose to take.”
 CHAPTER XXIX
JIM LASCELLES WRITES HIS NAME IN THE
VISITORS’ BOOK

THE husband-elect felt a perfectly legitimate curiosity concerning the

course to be adopted in this crisis by this eminently worldly wise,
hard-headed, and matter-of-fact diplomatist.
“Do you assure me positively that the man is a gentleman?” said
Caroline Crewkerne.
Cheriton ruminated. The term, as he understood it and as Caroline
interpreted it, was of a somewhat baffling complexity.
“Ye-es,” said he, after an interval of unusually weighty reflection; “I
should be inclined to say the young chap was by way of being one.”
“As that is your opinion,” said Caroline, grimly, “I shall speak a few
words to him myself upon the subject.”
Cheriton gave this determination the benefit of an ample measure of
his consideration.
“My dear Caroline,” said he, “it is either the worst thing you can do,
or it is the best.”
“I agree with you, Cheriton,” said Caroline Crewkerne. “And it all
depends upon the man himself. Tell Burden to look him up in
Walford.”
Walford preserved so much discretion upon the subject of Jim
Lascelles that, although several of his name were mentioned, neither
he nor his forbears were singled out for special notice. The practical
Caroline, having duly recorded the fact that “it was as she feared,”
desired to know whether Walford had anything to say upon the
subject of his mother. However, as no one at Pen-y-Gros Castle was
acquainted with the maiden name of Jim’s mother, Caroline’s
curiosity in regard to her also had to go unsatisfied. Nevertheless,
she had fully decided to speak to the presumptuous young man
upon the subject.
To that end John was dispatched after dinner that evening to the
lodgings of Mr. James Lascelles in Pen-y-Gros hamlet with the
compliments of his mistress and the request that Mr. Lascelles would
call at the Castle at noon on the morrow.
Mr. Lascelles sent back the information that he would be pleased to
do so. Yet no sooner had the gate of the cottage clicked behind the
emissary from the Castle than he repented, and it was only in
deference to the wisdom of his mother that John was not recalled.
Jim’s mother shook her head over him with sage indulgence.
“When will you learn, my son,” said she, “that old ladies who live in
Hill Street must be treated au grand sérieux by rising young painters
who live at Balham?”
“Yes, old lady, I suppose so,” said Jim, ruefully. “And if one James
Lascelles is ever to find the wherewithal to get back the Red House
at Widdiford, he will have to learn to keep his tongue in his cheek
and his back supple; and also learn how to stroke the fur of every old
cat that ever stuck somebody else’s coronet upon the panel of her
carriage.”
“For shame, my son!” said Jim’s mother.
And she bestowed an embrace upon James which he really did not
deserve.
Jim’s powers of resentment were unchristian and did him no credit,
but perhaps he would have shown less promise in his art had he
been less susceptible to the rubs of the world. That is the best that
can be said for him.
However, as the morning was wet, he did not mind so much that he
was due at Pen-y-Gros Castle at noon. He put on his carefully
brushed blue suit and the black silk tie that his mother had knitted for
him recently with her own fair hands, and at twelve o’clock precisely
he was seeking admittance at the gloomy portals. As he did so he
looked in vain for signs of the Goose Girl and the Muffin Girl. He
could not help speculating as to what the old heathen wanted him
for. Nothing pleasant, he would take his oath. Doubtless the Goose
had blabbed. If so, a warm quarter of an hour was before him. Yet he
felt that he should not mind that particularly. After all, the old
beldame was quite likely to receive as good as she gave.
John received him, and handed him over to Mr. Marchbanks himself,
who said, “Will you kindly come this way, sir?” in the manner that he
alone could say it.
Jim followed Mr. Marchbanks, after bestowing a somewhat
contemptuous glance at a daub in the entrance-hall which purported
to be the work of one Tintoret. A little further along, however, was a
Cavalier by Vandyck, which was more to his taste. He glanced at the
furniture also, which in its way was magnificent. It was of embossed
Spanish leather. At the head of the wide stone-flagged staircase up
which he was conducted, was a portière of Gobelin tapestry. Passing
through this, he was taken along a corridor containing good pictures
and bad, and mediæval weapons and suits of armor, until at last he
found himself in an extremely cozy room containing seductive
lounges and strewn with Turkish mats. And there, seated alone and
singularly upright in a high-backed chair, with a perfectly revolting
little dog sleeping at her footstool, was the old woman Jim Lascelles
so cordially disliked.
Jim was a little surprised that the old woman deigned to offer not two
fingers only, but the whole of her hand.
“What is in the wind, I wonder?” mused Jim, as he accepted it with
his best bow.
“It is good of you to come, Mr. Lascelles,” said the old woman, by no
means ungraciously. Remember there never was an old woman yet
who could not contrive to be agreeable if she really made up her
mind to be so. And Caroline Crewkerne was no exception to the
universal rule. “Pray be seated,” said she.
Jim Lascelles took the chair that was farthest from her ladyship.