T. RYAN GREGORY -- THE C-VALUE ENIGMA
TABLE OF CONTENTS
VOLUME ONE
Acknowledgments i
Table of contents v-xii
List of Tables xiii
List of Figures xiii-xv
Chapter One: Introduction to the C-value enigma
Abstract 2
Introduction 3
Genome size constancy and the C-value concept
4
Genome size variation and the C-value paradox
5
From paradox to puzzle 7
Mutation pressure theories 8
Junk DNA 8
Selfish DNA 11
Optimal DNA theories 12
The nucleoskeletal theory
12
The nucleotypic theory
13
Outline of the thesis 13
Concluding Remarks 15
Chapter Two: DNA content and the cellular phenotype
Abstract 20
Introduction: the importance of cell size
21
DNA content and cell size 22
The karyoplasmic ratio
22
Polyploidy and cell size
22
Genome size and cell size 23
Reptiles 24
Amphibians 25
Fishes 26
Birds 28
Mammals 31
Coincidence? 37
Size-dependent threshold
38
Overall increase in DNA content
38
Inability to delete extra DNA
39
Coevolution? 43
Nuclear size and the nucleoskeleton
43
Nuclear pores and RNA transport
45
Return and reversal of the karyoplasmic
ratio hypothesis 47
The pros and cons of coevolution
51
Causation? 54
Challenges to the nucleotypic theory
54
In support of the nucleotype
57
Previous models of nucleotypic influence
61
The nucleotide sequestration model
61
The division-initiation model
62
The gene-nucleus interaction model 65
Eukaryotic cell cycle regulation
66
DNA content and cell cycle length
68
DNA content and cell cycle control
71
Issues awaiting resolution
78
Concluding remarks 80
Effect versus function
80
Chapter Three: Genome size evolution in mammals and birds
Abstract 104
Introduction 105
Summary of the dataset 106
Statistical analyses 107
Patterns of variation in mammals and birds
109
Genome size and chromosome number 112
Genome size, cell size, and metabolism in mammals
114
Mammalian metabolism: analysis and
results 116
Mammalian metabolism: discussion
118
Genome size, cell size, and metabolism in birds
119
Avian metabolism: analysis and results
121
Avian metabolism: discussion
122
Genome size and flight 125
A causal connection? 125
Genomic baggage: lost or never loaded?
126
Genome size and developmental parameters
130
Sources of data 133
Avian development: dataset #1
134
Avian development: dataset #2
135
Mammalian development
138
Genome size, development, and body
size in homeotherms 139
Concluding remarks 141
Chapter Four: Genome size evolution in amphibians
Abstract 155
Introduction 156
Summary of the dataset 156
Statistical analyses 157
Patterns of variation 157
Genome size and chromosome number 159
Genome size, cell size, and metabolic rate in amphibians
162
Cell size and cellular metabolism
162
Genome size and metabolic rate
163
Cell size and metabolic rate
165
Genome size and developmental complexity
167
The threshold concept: genome size and development in
plants 168
Developmental complexity in amphibians 172
Developmental rate and constant complexity
172
Developmental process: direct development
175
Developmental process: neoteny
178
Developmental products: big genomes
and simple brains 184
Development in amphibians: a summary
187
Amphibian genome size and the hierarchy of evolution
189
Chapter Five: DNA quantification by Feulgen image analysis densitometry
Abstract 202
Introduction 203
DNA quantification: past and present 204
Densitometry 204
Fluorometry 206
Image analysis densitometry 209
Basic concepts 209
Guidelines for specimen preparation: vertebrates
211
Fishes 212
Amphibians 213
Reptiles 214
Birds 214
Mammals 215
Guidelines for specimen preparation: invertebrates
216
Crustaceans 217
Insects 219
Arachnids 223
Myriapods 224
Annelids 224
Molluscs 226
Echinoderms 228
Flatworms 228
Nematodes 229
Cnidarians 229
Miscellaneous invertebrates
230
Staining methods 231
The Feulgen reaction 231
Stain preparation 232
Staining protocol 233
Measurement protocol 234
Hardware and software
234
Microscope set-up and image capture
234
Choice of standards and calculation
of genome size 236
Concluding remarks 236
Chapter Six: Genome size evolution in terrestrial arthropods
Abstract 252
Introduction 253
Summary of the dataset(s) 254
Insects: previously published data
254
Insects: new genome size estimates
254
Spiders 255
Other arachnids 257
Myriapods 257
Patterns of variation in insects 258
Blattaria 258
Coleoptera 259
Collembola 264
Dermaptera 264
Diptera 264
Embiidina 268
Ephemeroptera 268
Hemiptera 268
Hymenoptera 271
Isoptera 272
Lepidoptera 272
Mantodea 274
Odonata 274
Orthoptera 274
Phasmida 276
Plecoptera 278
Siphonaptera 278
Thysanura 279
Trichoptera 279
Patterns of variation in arachnids 279
General patterns in spiders
279
A note on the spider mite
281
Patterns of variation in myriapods 281
Developmental complexity in insects: more on metamorphosis
282
Concluding remarks 286
Chapter Seven: Macroevolution, hierarchy theory, and the C-value enigma
Abstract 300
Introduction 301
Macroevolutionary theory for neontologists
302
What is macroevolution?
302
Critiques of the Modern Synthesis
304
Reductionism in biology
309
Group selection: new and improved
and no longer naïve 312
The concept of individuality
315
Punctuated equilibria and species
as individuals 318
Species selection in principle and
in practice 321
Aggregate versus emergent characters
323
Emergent fitness versus the effect
hypothesis (the Lloyd-Vrba debate) 325
Selection versus sorting
328
Hierarchical macroevolutionary theory:
a summary 330
Molecular macroevolution 332
Are genomes “individuals”?
332
The necessity of hierarchy theory for understanding genomes
(and vice versa) 337
Group selection and the origin of
the genome 337
Selfish DNA and the necessity of hierarchy
339
The C-value enigma from a hierarchical perspective
342
Genomes as phenotypes and genotypes
343
The evolution and ecology of transposable
elements 346
Selection, sorting, and genome size
351
Stasis and DNA constancy
353
Genome-level processes and the major transitions in evolution
356
Concluding remarks 365
References for Volume One 368
VOLUME TWO
Appendix 1 – Reptile erythrocyte sizes 444
Appendix 2 – Amphibian erythrocyte sizes 447
Appendix 3 – Fish erythrocyte sizes 457
Appendix 4 – Bird erythrocyte sizes 468
Appendix 5 – Mammal erythrocyte sizes 485
Appendix 6 – Mammal genome sizes 507
Appendix 7 – Bird genome sizes 539
Appendix 8 – Amphibian genome sizes 555
Appendix 9 – Reptile genome sizes 602
Appendix 10 – Fish genome sizes 628
Appendix 11 – Insect genome sizes (database) 722
Appendix 12 – Insect genome sizes (original data) 745
Appendix 13 – Spider genome sizes 764
Appendix 14 – Crustacean genome sizes 772
Appendix 15 – Mollusc genome sizes 792
Appendix 16 – Annelid genome sizes 808
Appendix 17 – Flatworm genome sizes 819
Appendix 18 – Echinoderm genome sizes 823
Appendix 19 – Nematode genome sizes 827
Appendix 20 – Miscellaneous invertebrate genome sizes 829
References for Volume Two 837
LIST OF TABLES
Table 3.1 – Variance distribution of genome size in mammals and birds
144
Table 3.2 – Genome size, cell size, and metabolic rate correlations in mammals
145
Table 4.1 – Variance distribution of genome size in amphibians
192
Table 4.2 – Genome size and developmental rate in amphibians
193
Table 5.1 – Summary of slide preparation methods for animal specimens
238-240
Table 5.2 – Outline of Feulgen staining protocol 241
Table 5.3 – Explanation of steps in Feulgen staining protocol
242
Table 5.4 – Checklist of steps in image analysis protocol 243
Table 6.1 – Summary of hexapod C-value measurements 289-290
LIST OF FIGURES
Figure 1.1 – C-value ranges in eukaryotes 17
Figure 1.2 – Sequence composition of the human genome 18
Figure 2.1 – Red blood cells of vertebrates (Gulliver 1875)
82-83
Figure 2.2 – Red blood cells of polyploid salamanders 84
Figure 2.3 – Genome size versus erythrocyte size in vertebrates
85
Figure 2.4 – Red blood cells of vertebrates (photos) 86-87
Figure 2.5 – Genome size versus erythrocyte size in reptiles
88
Figure 2.6 – Genome size versus erythrocyte size in amphibians
89-91
Figure 2.7 – Genome size versus erythrocyte size in fishes (preliminary)
92
Figure 2.8 – Red blood cells of a teleost and a lungfish (photo)
93
Figure 2.9 – Genome size versus erythrocyte size in fishes (Hardie 2002)
94
Figure 2.10 – Genome size versus erythrocyte size in birds 95
Figure 2.11 – Genome size versus erythrocyte size in mammals
96
Figure 2.12 – Red blood cells of mammals (photos) 97
Figure 2.13 – Genome size versus epithelium cell size in mammals
98
Figure 2.14 – Genome size versus sperm cell size in mammals
99
Figure 2.15 – Cell cycle regulation in eukaryotes 100-101
Figure 2.16 – The Rabl configuration of nuclear DNA 102
Figure 3.1 – Genome size distribution in mammal families 146
Figure 3.2 – Genome size distribution in bird families 147
Figure 3.3 – Genome size distribution in mammals and birds 148
Figure 3.4 – Genome size versus chromosome number in mammals and birds
149
Figure 3.5 – Genome size versus metabolic rate in birds 150
Figure 3.6 – Genome size distribution in bird families (flight ability)
151
Figure 3.7 – Genome size and flight ability in birds 152
Figure 4.1 – Genome size distribution in amphibian families
194
Figure 4.2 – Genome size versus chromosome number in amphibians
195
Figure 4.3 – Genome size versus metabolic rate in amphibians
196
Figure 4.4 – Erythrocyte size versus metabolic rate in amphibians
197
Figure 4.5 – Genome size and developmental lifestyle in plants
198
Figure 4.6 – Genome size and developmental lifestyle in amphibians
199
Figure 4.7 – Nucleated and enucleated erythrocytes of salamanders (photos)
200
Figure 5.1 – Blood smear preparation protocol 244
Figure 5.2 – Feulgen image analysis standard curve 245
Figure 5.3 – Hepatocyte, leukocyte, and erythrocyte nuclei (photos)
246
Figure 5.4 – Stain density versus DNA compaction level (photo)
247
Figure 5.5. – Sperm and haemocyte nuclei from insects (photos)
248
Figure 5.6 – Sperm bundle dispersion in moths 249
Figure 5.7 – Sperm and blood cell nuclei from annelids 250
Figure 6.1 – Genome size distribution in beetle families 291
Figure 6.2 – Genome size distribution in dipteran families 292
Figure 6.3 – Genome size distribution in hemipteran families
293
Figure 6.4 – Genome size distribution in lepidopteran families
294
Figure 6.5 – Genome size distribution in orthopteran families
295
Figure 6.6 – Genome size distribution in spider families 296
Figure 6.7 – Genome size and metamorphosis in insects (order means)
296
Figure 6.8 – Genome size and metamorphosis in insects (order ranges)
296
Figure 7.1 – Genomes in an expanded biological hierarchy 367