ABBREVIATIONS

A list of the more commonly-used abbrevia• cVg-I, Vegetal mRNA or protein in early chick tions other than those in figure legends. Mem• embryos bers of gene families (e.g. BMP-4, Hoxa-I) are DIl, distal-less gene in Drosophila listed under the gene family (BMP, Hox) and Dlx, the vertebrate orthologue of DII not separately. DNA, deoxyribonucleic acid dpp, the decapentaplegic gene in Drosophila, abd-A, abdominal-A genes of the bithorax a member of the TGF-~ superfamily complex D-V, dorso-ventral axis or dorso-ventral Abd-B, abdominal-B genes of the bithorax polarity complex ECM, extracellular matrix AER, apical ectodermal ridge of tetrapod limb EDB, evolutionary developmental biology buds EDTA, ethylendiaminetetraacetic acid, a AmHNF-3, hepatic nuclear factor-3 (HNF-3) chelating agent gene in Branchiostoma (amphioxus) EGF, epidermal growth factor AmphiEn, the orthologue of the engrailed gene EGF-R, epidermal growth factor receptor in Branchiostoma (amphioxus) En, the engrailed homeobox-containing gene AmphiHox-l-AmphiHox-12, Hox genes of Bran• in Drosophila chiostoma (amphioxus) eng, the vertebrate orthologue of Drosophila AmphiOtx, Branchiostoma (amphioxus) mem• en ber of the orthodenticle (otd) gene family Er, repeated epilation mutant mice in which ANT-c, the antennapedia complex of Dro• both limb and tail ridges are abnormal sophila homeotic genes eve, even-skipped, a pair-rule gene in Dro- antp, the antennapedia gene in Drosophila sophila A-P, antero-posterior axis or antero-posterior ey, eyeless mutation in Drosophila polarity FGF, fibroblast growth factor ATPase6, adenosine 6'-triphosphatase GDF, growth differentiation factors bFGF, basic fibroblast growth factor Gli2, a zinc finger gene in mice BMP, bone morphogenetic protein, a member Her-I, the zebrafish orthologue of the Dro• of the TGF-~ superfamily sophila pair-rule gene Hairy BX-C, the bithorax complex of Drosophila HNF-3, hepatic nuclear factor-3, a DNA• homeotic genes binding protein CAM(s), cell adhesion molecule(s) Hox, vertebrate genes related to Drosophila cDNA, complimentary DNA ANT-C and BX-C gene clusters ch, congenital hydrocephalus mutation in mice HrPax-37, Pax gene of the ascidian Halocynthia chn, chinless mutation in zebrafish roretzi CJMs, cell junctional molecules IGF, insulin-like growth factor Clx, clock genes in Caenorhabditis elegans Krox-20, a zinc finger protein cSnr, chick member of the snail family of L-CAM, liver cell adhesion molecule Drosophila genes Lef-I, lymphoid enhancer-binding factor-l 404 Abbreviations lin, cell lineage abnormal genes in SAM(s), surface adhesion molecule(s) Caenorhabditis elegans ScI, scalloped wings, modifier of Rop-l L-R, left right axis or left-right polarity Ser, Sex combs reduced, a homeotic gene m3, a central tarsal bone in salamanders Sey, small eye, a mutation of Pax-6 mRNA, messenger ribonucleic acid ss., sections, referring to other sections in the Msh, muscle segment homeobox gene in book Drosophila shh, sonic hedgehog gene Msx, orthologues of Drosophila Msh in verte• Six6, the mouse orthologue of Pax-6 brates sog, short gastrulation gene in Drosophila mya, million years ago TGF-~, transforming growth factor-beta MyoD, myoblast determination 1 protein Trx-G, trithorax response element of such expressed only in muscle cells genes as Scr NADH1, nicotinamide adenine dinucleotide ub, ultrabithorax gene in Drosophila N-CAM, neural cell adhesion molecule Uro-2, Uro-ll , ascidian genes that encode a Otx, vertebrate members of the Drosophila DNA-binding gene orthodenticle (otd) gene family vestigial tail (vt), mutant mice lacking a tail (p), premature death mutation in Ambystoma ridge mexicanum Vg-l, vegetal mRNA or protein located in the Pax, mouse member of Drosophila paired box vegetal pole of Xenopus blastulae. genes wnt, a family of cysteine-rich glycoproteins in Pc-G, polycomb response elements of such vertebrates, named from wingless (wn) and genes as Scr. integrated (t), Drosophila and vertebrate seg• P-D, proximo-distal axis or proximo-distal ment polarity genes polarity Xbap, bagpipe gene in Xenopus pdm, a gene involved in initiation of wing XVent-2, a novel homeobox gene in Xenopus primordia in Drosophila Xwnt, Xenopus member of the Drosophila wing- RA, retinoic acid less gene family Rop-l, resistance gene to dieldrin ZPA, zone of polarizing activity in limb rRNA, proposed ribosomal ribonucleic acid buds s, section, referring to another section in the book REFERENCES

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References to figures are in bold; references to tables are in italics. Species and gene names are also italicized.

Abd-A, see Abdominal-A gene Ambystoma maClllatum 182, 380 vertebrates 85, 86 Abd-B, see Abdominal-B gene Ambystoma mexicanum 138 (n6), Annular ligament 183, 200-1 Abdominal-A gene 147, 146-7, 290 167, 182, 199, 208 (n5), 380, Anomalocaris canadensis 47 Abdominal-B gene 147,146-7 404 ANT-c, see Antennapaedia Academie des Sciences debate 62-7 premature death mutation complex Acanthocephala 20, 29 in 199 Antennapedia complex 146-7, Acanthostega 259-fiO, 262 Ambystoma puncta tum 183, 200 147,150, 162 (Box 10.1) Acipenser 36 (n12), 371 Ambystoma texanum 125, 291 see also Homeotic genes Acoelomate animals 20, 28, 29 Ambystoma tigrinum 125, 200, 290- Antennapaedia gene 146-7 Acorn worms, see Hemichordata 1,292 (n1) Antero-posterior polarity Acropora formosa, zootype of 229 Ambystoma tigrinum mavortium Drosophila 188, 235 Activation of the egg 129-30 303 genetic basis of 188 artificial 132 Ambystoma tigrinum nebulosum 303 in limb development 184, 185, Activin-A 156, 158 cannibalistic morph 303 186 Activin-B 158 AmHNF-3245 Xenopus 188 Adaptation 305 (n1) Amia 31 Antp, see Antennapaedia gene in architecture 63 (Box 4.3) Amiskwia sagittiformis 47 Aortic arches, patterns in Darwin and 75-6,217 AmphiEn rabbit 202, 202 to diet 103, 272 in amphioxus cerebral Apical ectodermal ridge 184-fi, and environmental change 297- vesicle 246, 403 184,185 9,307 AmphiHox 244, 244-fJ see also Limb development exaptation 281 AmphiOtx 345 Arabidopsis 150, 153 (n10) and function 60,281 Amphioxus, see Balanoglossus Archaea 17,18 and genetic assimilation 315-17 Analogy 75 Archaeocyatha 23 and key innovations 218, 277, Anatomical plans, see Body plans Archaeopteryx 255, 265-6, 287 283-fi Andrias 204, 381 Archetypes 69-80,74,94,306 larval 136, 232--4, 353-8 Anguilla rostrata 36 (n12) see also Unity of type and plasticity 301 Animal Kingdom 17-18,19-22 Aristotle preadaptation 281, 318 axis specification 358 and development 70,112 to predation 300-2 brain development 345-6 and epigenesis 5 to seasonal change 102, 298-9, and other kingdoms 17-18,18 and preformation 5 330 conserved Hox code 242 and unity of types 57-9,64 and size 225 (Box 14.1) conserved segmentation Arrow worms, see Chaetognatha types of 281,297-8 mechanisms 231 Artemia franciscana 276, 341 see also Genetic assimilation embranchements 61-2,70,81 Arthropods Adaptive radiations 218 eye development 344-5 and annelids 85, 188 AER, see Apical ectodermal ridge grades based on germ arthrotype as phylotypic Agassiz, J. L. R. 10, 76, 89 (n4) layers 81, 83 stage 228 see also Recapitulation larvae as surrogate blastula as phylotypic stage 228 Agmata 23 ancestors 232 in Burgess Shale 40 Agnatha 22, 256, 341 phyla of 18-26 conservation of Hox code 221, origins of 34, 241 similar embryological 346 see also Jawless vertebrates development 69, 129 in Ediacara fauna 24 Alligator mississippiensis 119 (n3) synapomorphies of 33, 227 features 21-2, 29 Allometric engineering 315,319 zootypes 229-31,397 genes in common arthropod• (n2) Animal phyla annelid ancestor 188 Allometry 315 (Box 19.1), 396 see Super phyla and individual genes in common arthropod• Ambystoma 183, 186, 175 (n30), phyla chordate ancestor 241-2, . 187, 306 (n12) Annelida 21, 29, 226 257,397-8 hybrids 125 transformation to pattern of differentiation 226 480 Index

Arthropods (continued) Balancers, induction of 290--1, 291 and origin of germ layers 81 relationships 49,51-2,54 (n4) see also Ambystoma mexicanum see also Cleavage 79 Balanoglossus 22,85,87-8,90 BMPs, see Bone morphogenetic see also Drosophila; Trilobites; (n25,26), 231 proteins Uniramia Hox genes of 245-7 Body plans Asbestopluma 96 stomochord 88 and homeotic genes 144, 147 Ascidians Balfour, F. M. 83-4,98,90 (n19) insect 144-7 BMP-7 in 171 and larvae 232-4, 238 (n15-16) rna ternal effect genes and 144 features 22 Balfour's law 139 (nIl) and primary embryonic neural induction 171 Barry, M. 71 axis 155-9 notochord induction 159 Basic fibroblast growth factor segmentation genes and 144-5 tadpole 85,85--{) activates Brachyury 158 see also Bauplane; Homeotic and vertebrate ancestry 85,361 induces neural crest 169, 170 genes (nI6) (Box 10.3) Bolyeria 283, 292 (n5) see also Molguia spp.; induces neural ectoderm 169, Bolyerine snakes 283, 292 (n5) Urochordates 170 (Box 10.3) Bombina 355, 367 Asplanchna brighlwelli 300-1 mesoderm induction 156-8, Bone morphogenetic proteins Aslatotilapia elegans 272 157,161 in AER 192 Astraspis 39 Basilosaurus isis 289 and A-P axis 188 Astyanax fasciatus (Mexican cave Bateson, W. 84, 87-9 equivalent to decapentaplegic of fish) 207 Bauplane Drosophila 151-2 Atavisms constraints and 99-101 in enamel knot 192 of carpals and tarsals 204-5 levels of 95--7 in notochord 192 and homology 341 lizard 97 in ZPA 192 insect prolegs as 290 maintenance of 106-7 BMP-2 and potential for nested 97 limb shape 187-9 evolution 204-5, 251 (n9) of phyla 18, 28 tooth induction 191 thigh muscles in birds 290 of turtles 269-70 BMP-4 three-toed horses 288-9 see also Body plans; Unterbaupliine; and apoptosis 171, 189 whale hindlimbs 289-90 Woodger, J. H. and dermomyotome 164,191 Australochelys africanus 269 Bdellostoma stoutii 126 determines ventral 152, 157 Autonomization 311 Beer, G. R. de limb shape 187-9 see also SchmaJhausen, 1. 1. and homology 10,341-4,347 and mesoderm Autonomous specification, see Cell Beetles, see Schistocerca; Tribolium induction 156--7, 157 fate bFGF, see Basic fibroblast growth and msx-l 191 Avian factor and neural crest blastodisc 134 Bicalyx gene 150 induction 170--1,191 ontogeny, duration of 366, 366-- Bichirs 32 and neural induction 159-60 7,368 Bicyclus anynana 320 (n13), 330--1, and tooth induction 191, 192 see also Birds 332 (n18) BMP-7 Axolotl, see Ambystoma mexicanum Bilateral symmetry 20-2, 28, 29 and ascidian neural Aysheaia pedunculata 40, 42, 43, Biogenetic law, see Baer, K. E. von induction 243 53 Biological homology, see and neural crest Homology induction 170--1,191 Baer, K. E. von 69-70 Biological species, see Species Bonnet, Charles 6, 8 biogenetic law 337 (Box 21.1) Biological time 371 Brachionus calyciflorus 300-1 and phylogenetic Birds Brachiopoda 21, 29, 226 systematics 337 (Box 21.1) evolution of 2, 65-7 and morphospace 50 early embryonic stages see also Avian Branchiostoma 243-4, 368, 403 conserved 95,135,354 Biston betularia Brachyury gene embryonic archetypes 70-1, 88, Bithorax complex 146--7, 147, 162 in ascidians 244-5 230 (Box 10.1) and notochord induction 158-9 germ layers 81, 112 see also Genetic assimilation; and tooth development 172 influence on British Homeotic genes Bryozoans, see Ectoprocta embryologists 69, 71-7, 95 Blastodisk 134-5, 134 Buffon, G. L. 58-9, 61, 67 (n2) homology and development 71 Blastula Bufa 380, 382 laws of development 69-2, 84, as embryonic stage 81, 132-4 Burgess Shale fossils 39-54, 206 89 (n2), 95, 106 as Haeckel's primordial arthropods of 40 see also Recapitulation stage 80,82 assignable to phyla 40-9 Index 481

and Cambrian explosion 32, 34 Cell lineages Cleavage not assignable to phyla 46-9,54 in dentary bone 325, 327 of eggs 132 (n7) in direct developing patterns and super phyla 29, and Ediacaran fauna 23 echinoderms 258,261 (n13) 135, 139 (n15) not unique 52 in Caenorhabditis elegans 235-6, see also Radial cleavage; Spiral Butterfly eyespot patterns 330-1 379 cleavage BX-C, see Bithorax complex in larvae 236-7 Clock genes 371, 373 (n8) and patterns of embryogenesis see also Timing of development Cadherins, see Cell adhesion 235 Cnidaria 19,29,36 (n5), 117, 130, molecules in Styela partita 115 131,226 Caecelians 124, 138 (n2), 381 variability within 220-1 Coelacanth 28, 30, 32, 36 (n12) Caenogenesis 237 (n14) Cement gland, development Coelenterates, see Cnidaria Caenorhabditis elegans of 355, 369 (n8) Coelomate animals 21-2,28-9 cell determination 114,379, 390 Central nervous system 161-4 Coiter, Volcher 112 (n12) see also Neurulation Colony formation 109 (n11) cooperation between genes 278 Cephalocarida 23 Comb jellies, see Ctenophora (n15) Cephalochordata 44-6 Competence Lin genes 379 Hox genes and 243-5 see Induction as model organism 125 patterns of differentiation 226 Complexity 9,223-6 number of cell types 225 phylum definition 22, 29 hierarchy 224 type 1 embryogenesis 235, 236 relationship to chordates 24, 27 number of cell types 224-6 Cambrian explosion 32, 34 relationship to conodonts 37 number of genes 226 CAMs, see Cell adhesion see also Pikaia gracilens Condensations molecules Cephalopods of dentary bone 325-6 Canadia spinosa 49 see Sepia as fundamental developmental Canadaspis perfecta 40 Chaetognatha 22, 29 units 325-6, 332 (n7), 373 Canalization Chambers, Robert 72 (n6),400 of development 104, 115, 201-5, author of Vestiges 72-3, 89 (n5) and heterochrony 377-8 201, 209 (nlO), 311 Chancelloria eros 47 importance of size 372 (n8), and selection 104,201,310, 311, Chaoborus 301 377-8 317-18 Cheek pouches 12, 284-5, 385 and inductive tissue see also Stabilizing selection Chelonia midas 270, 271 interactions 332 (n7), 390 Cannibalistic salamanders 303, Chelydra serpent ina 165, 269, 270-1 (n7) 306 (n12) Chengjian formation 45, 52 and regulation 390 (n6) Carapace, evolution of 267-71, Chlamydomonas 219 Conditional specification, see Cell 269,271 Chordates fate Carassius carassius 302 Hox genes and 241-5 Confuciusornis 266 Carpal bones, pattern of 202, 204 origin of 239-44 Conodont elements 24, 25, 26 Carpenter, W. B. 71-2,89 (n5) phylum description 22 Conodonts 24, 36 (n7), 44 Cartilage relationships 27 relationships 27 induction of 198, 386 Chordin Constraints in invertebrates 105, 109 (n21) in Xenopus 151, 152, 153 (n12) cellular 104-5 secondary 180,197,317-18 Chromatin structure 118, 120 (n9) constructional 101 see also Meckel's cartilage Chromosome inactivation 119, developmental 103-4 Cathaymyrus diadexus 45-6 120 (n11) functional 100-2 Cell adhesion molecules 178-9, Cichlasoma managuense 303 and generation of Baupliine 220 Cichlid fishes genetic 102-3 see also Liver-cell adhesion diet and tooth morphology 272 maintenance 103 molecule; Neural-cell speciation 271-3 maternal 105, 109 (n22) adhesion molecule pharyngeal jaws 271-4,272,318 mechanical 109 (nll) Cell condensations, see see also Aslaloti/apia elegans; metabolic 105, 109 (n20) Condensations Cichlasoma managuense; pattern 100-2, 109 (n12) Cell fate Oreochromis mossambicus process 101-6 autonomous specification Clona 174,244,252 (nS) size and 101, 198 (n20) of 104, 226, 235-6 CJMs, see Cell junctional structural 100 conditional specification of 104, molecules see also Baupliine 235-6 Cladistics 51, 54 (n9), 333 (Box Continuity of the germ plasm see also Caenorhabditis elegans 21.1) 142,152 (n1)m, 215 (Box 13.1) Cell junctional molecules 179 Clarkia concinna 150 see also Weismann, A. 482 Index

Cope's law 14 and genetic constancy 306 in echinoderms 128, 136, 357-8, Cope's rule 14,224,225 (Box (n9) 358 14.1),237 (n4) heartbeat 367 Discoglossus pictus 198, 208 (n3) Cortical inheritance 117 Darwin, Charles Distal-less gene Cortical rotation 131 use of embryological in branchial arch ectoderm 247 Crania tes 22, 241 evidence 77,90 (n11) and butterfly eyespot excludes hagfishes 21, 241 evolution 8-9, 13, 75-6, 77 focus 330-1 origin of head 239-41, 245-7 views on homology 75-6 in cement gland 355-6 Creeper mutant 189 (n2) see also Archetypes; Homology; and echinoderm body plan 221 Crossveinless, see Genetic Unity of type in Eleutherodactylous coqui 355-6 assimilation Decapentaplegic protein in migrating cells of Crustacea and A-P axis 188 amphioxus 245 larvae 78, 79, 138 and BMP 151-2 in migrating neural crest Muller, F and 78, 340 and D-V axis 151 cells 355 zoea larva 79, 79 Deformed homeotic gene 146-7 mutation and branchial arch Ctenophora 19,29,43, 117,226 Dentary bone 285 defects 247 Curly leaf gene 150, 153 (n10) genes and 327 patterning of the forebrain 355 Cuvier, Georges Gli2 zinc finger gene and cell at tips of appendages 221 debate with Geoffroy xvi, 62-7, lineage 327 DlI, see Distal-less gene 398 Goosecoid and cell lineage 327 DNA, see Methylation embranchements 61-2,70,81 Lef-l and cell lineage 327 Dobzhansky, T. 12, 14 and Sepia 64 and model for morphological Dohrn, A. 84-7 C-value paradox 102, 109 (n15) evolution 323-6, 324, 325, Dollo's law 14,281,186-7 see also Genome size 327 Dorso-ventral polarity Cycliophora 18, 20, 23, 29 msx genes and cell lineage, in amphibians 131 Cyclopmorphosis 300 327 BMP-4 and 152, 157 cannibalistic salamanders 303, and separate cell lineages 327 in Drosophila 185, 235 306 (n12) TGF-~, and cell lineage 327 of eggs 129 in carp 302 Dentine 189, 260 in insects and vertebrates 150- in Daphnia 301-2,305,306 (n6) Dermal skeleton 260 2 ecology and 300-5 Dermestes 136, 146 and limb development 185, 186 in geometrid moths 303-4 Deuterostome animals 22, 28, 29, in type 3 embryogenesis 235 in rotifers 300-1 30 Double assurance 109 (n13), 181, in sticklebacks 305 and vertebrate evolution 240 195 (n11) Cyclostomes Developmental evolutionists 213- Dpp, see Decapentaplegic protein amphioxus as degenerate 87 15 Drosophila as archetype of vertebrate Developmental time, see Timing of adb-A gene reduces limb skull 74 development development 290 as degenerate vertebrates 87 Developmental units, see atavism 287 see also Agnatha; Hagfish; Fundamental bagpipe gene 200 Lampreys developmental units bristle patterns 287, 316, 326 Cynolebias 135-6, 139 (n14) Diastylis 138, 139 (nl7), 384 clock genes 371, 379 Cytula 80, 82 Didelphis 388, 391 (n29) determination of germ Digits cells 142-3, 153 (n3) Danaus plexippus 331 evolution of 260-1,277-8 (n7), eight homeotic genes 221 Danio rerio 278 (n18) eyeless mutant 315-16,344-5 axial specification 160,173 (n11) numbering 261 (Box 16.1) fifty cell types 226 blastomere variability 220, reduction of during four-winged 149 determination of cell fate 236 evolution 288 heat shock 398,365 double blastoderm eggs 139 see also Homology homeotic genes 118, 147, 153 (14) Dinomischus isolatus 47-9, 49 (n5,6), 162 (Box 10.1), 221, fate map 222 (13) Dinosaur origin of birds 266-7, 229,398 fin 263 277-8 (n7) length of cell cycle 102 Hox genes of 245, 263 Dipleurula larva 22 a long-germ band insect 136 phylogenetics 102, 125 Dipodomys 384, 385 maternal effect genes 144, 153 staging 368 Direct development (n5),322 Daphnia in amphibians 129, 134, 136, meroistic ovary 146 cyclomorphosis 301-2,305,306 354-7,355,356 mitotic cycle and 102 (n6) in ascidians 128, 358-60 as model organism 125, 397 Index 483

segmentation 231,275,319,397 Enamel knot 191-3,192 tooth development 190 segmentation genes 144-5 see also Tooth induction transmission electron sog and 151-2,152, 153 (n12) Enameloid 378 microscopy of 179 two-winged mutant 275 Engrailed Eptatretus stoulii 126, 245, 247 type 3 embryogenesis 234-6, in amphioxus 246 Equus 288,288 235 branchial arch muscles of Eriptychius 39 see also Genetic assimilation; lamprey and zebrafish 258 Eucidaris tribuloides 136 Homeotic genes; Homeotic and echinoderm body plan 221 Eukaryia 17, 18 mutations ectopic expression in Eumetazoa 19,29 Drosophila melanogaster 206, 308, Drosophila 275 Eve, see Even-skipped gene 316 in mandibular arches 258 Even-skipped gene 146,229 Drosophila pseudoobscura 318 at mid-hindbrain 161, 258 Evolution Dugesia gonocephala 313 and segment identity 144,231, beyond biology 10-11 Dwarfism 377 275 as change 8-9 and site of limb formation 187- definition 13 Ecdysis 28 8 as genetic change 11-12 Ecdysozoa 28,36 (n9) ultrabithorax regulated by 275 as hierarchy 12-13 Echinoderms 22, 29 Ensatina eschscholtzii 202, 204 history of the term 3 see also Direct development Entoprocta 20, 29 origin of the term 4-7 Echiura 21, 29 Eohippus 288, 288 as population genetics 11-12 Ecology Epidermal placodes, see Placodes as preformation 4-7 and agnathan ---.. gnathostome Epigenesis as progress 9-10 transition 7, 256 contrasted with epigenetics as unfolding 4-5 and cichlid speciation 271-4 113-14 see also Macro-, Mega-, decoupled from morphology and preformation 5, 112-13 Microevolution 218 Epigenetic burden 214 Evolutionarv causation 4, 15 evolution as the control of Epigenetic cascades 177,194 (n2), (n 1,2), 108 development by 294, 300, 201 see also Functional causation 305,389-9 and kidney development 193 Evolutionary novelties and genetic assimilation 314 and oral development 198 and adaptation 218-19 and heterochrony 379-83 and tooth development 189-93 and heterochrony 378 and inductive interactions 300 Epigenetic traps 215 and heterotopy 388 larvae and 353-4, 357 Epigenetics and speciation 217-18 larval loss 357-8 definition 113-14 see also Key innovations and origin of phyla 35, 53 and ecology 300-5 Exaptations 281 and pharyngeal jaws 257 and genetics 114-15 Excess structural capacity 101 and seasonal path analysis model 329 External causation, see polymorphism 300-5 as regulator not replicator 215 Evolutionary causation size and 105 (Box 13.1) Eyeless gene in Drosophila 315, tracked by morphology 35, 50- see also Inheritance systems 344,344-5 1, 218, 298, 323 Epithelia 105, 177-8,178,180 from water to land 259 Epithelial-mesenchymal Feathers, evolution of 265-7 Ectoprocta 21, 29, 51, 226 interactions Fertilization 129-32 Ediacaran fauna 24, 36 (n 5,6) bone induction 180-1, 195 (n8) timing of and stages of EGF, see Epidermal growth factor cartilage induction 180, 385-7, oogenesis 131 Elephants, see Elephas falconeri; 386 FGF, see Fibroblast growth factors Loxodonta africana cellular mechanisms 178-81 Fibroblast growth factors Elephas falconeri 381 diffusion-mediated 181 activate posterior homeotic Eleutherodactylus coqui matrix-mediated 180-1, 195 genes 162, 186 basic features of embryos 355, (n4) induce limbs 185-6 356 cheek pouches 384-5, 385 FGF-2 functions as AER 185, dll expression in 355-6 feathers 266-7 187,189 thyroid axis 360 (n5) generation of new tissues 268 FGF-4 see also Direct development heterochrony and 378, 380, 390 and BMPs in limb buds 189 Embryogenesis, patterns of 235 (n8) and Msx-1 192 Embryonic induction, see mammary gland 181 and shh in limb buds 187, Induction origin of novelties 286, 384-5, 192,192 En, see Engrailed 378,380 in enamel knot 192-3,192 Enamel 189, 260 sense organs 181-3,195 (n13) in notochord 192 484 Index

Fibroblast growth factors (continued) and origin of germ layers 81 change 328-9 in ZPA 192 Gastrulation 132 phenotypic plasticity as FGF-8 Gegenbaur, K. 87 variance accounted for mid-hindbrain boundary 161 Gene duplication by 299 tooth induction 191 of brachyury in amphioxus 245- as reaction to environmental and mesoderm induction 156--8, 6 perturbation 329 157,161 of homeotic genes 242, 244, 398 effect of temperature of 320 Fin ~ limb transition 251Hi4, 259 of paralogous genes 150 (B 9.1), (n13) Hox genes and 262-3 339 Geoffroy, E. Saint-Hilaire Fisher, R. A. 12 at the origin of the craniates and debate with Cuvier xvi, Flatworms, see Platyhelminthes 257 62-7,396 Fluctuating asymmetry 205-8, 209 at the origin of the influence in Britain 71-7,89 (n 15-16) vertebrates 245-6 (n3) Comparative studies 206-7 Genetic assimilation principle of connections 59, 67 and developmental adaptation and 315-17 (n4) constraints 368 of behaviour 314,317 and teratology 60, 112 genetic basis 208 of Bithorax 308-10,317 union of invertebrates and and insecticide resistance 208 of crossveinless 308 vertebrates 59-60 Mexican cave fish 207-8 and Dugesia gonocephala 313 see also Homology; Idealistic Forbes, E. 76, 77 (Box 5.1), 237 and Gasterosteus aculeatus 313 morphology; Unity of the (n11) and genetic fixation 316 type Form and function 62-3 (Box 4.3) genetics of, 309-13 Geomyoid rodents 384-5, 385 Fossils, taxonomy of 51-2 and Limnaea 313-14, 317 Germ-band stages Fringe gene and P-D axis 188 a mechanism for 310-11,311 intermediate 137, 137 see also Radical fringe in nature 313-15 long 137, 137, 146, 235 Fugu rubripes 245 and phenocopies 309, 319 (n2) short 137, 137 Function polygenic basis of 313 and type 3 embryogenesis 235 as determinant of form 622-3 and Rana sylvatica 313-15 Germ cells (Box 4.3) and secondary cartilage determination of 141--4 Functional causation 4,108 selection and 309-11, 314, 317, in amphibians 142--4 Functional morphology 59, 194 319 in Drosophila 142-3 (n3) and xerophytic plants 314 migration of 143 Fundamental developmental units see also Canalization of see also Continuity of the germ condensations as 325-6, 332 development; Waddington, plasm; Germ plasm; (n7), 373 (n6), 400 C. H. Somatic embryogenesis in morphology 321-2,400 genetic covariance 103 Germ-layer theory 81-3,90 (n18) Fundulus heteroclitus 245, 368 Genome size 19, 102, 109 (n15) Germ layers Fungi 17, 18, 104 see also C-value paradox Baer, K. E. von and 28, 81, 112 Genomic imprinting 119,120 Balfour, F. M. and 83--4 Gallus domesticus 125, 368 (n11) diploblastic animals and 29, 81, Gap genes 144 Genotype 399 83 Garstang, W. 13 by environment interactions and heterotopy 383 Gasterosteus aculeatus 305, 313 318-19 Huxley, T. H. and 80-1 Gastra!a theory 79-81, 353 canalization builds unexpressed Lankester, E. R. and 83 see also Haeckel, E. variability in 201, 310 neural crest as fourth 28,29, 83, Gastroneuralia 28, 29, 86 embryo transfer between mice 169 Gastropods of different 328 Pander, C. H. 81, 112 and morphospace 50 and fluctuating asymmetry 208 and super phyla 28 origin of torsion in 276-7 no one-to-one correlation with triploblastic animals and 29, 81, Gastrotheca 134, 360 (n4) phenotype 114,321,399 83 see also Direct development and phenotype of the gene 117- Germ plasm Gastrotheca ceratophrys 354 18 distinct from soma 4,141-3 Gastrotheca plumbae 136, 354 and phenotypic plasticity 299- Weismann, A. and 142 Gastrotheca riobambae 136, 354, 355 300,302,308 see also Continuity of the germ Gastrotricha 20, 29 response to environmental plasm; Germ cells Gastrula signals 307, 310, 313, 316 Gerris costae 368 as embryonic stage 81, 132, 134 Genotype by environment Gerris odontogaster 103 as Haeckel's primordial interactions Girardia biapertura 96 stage 80,82 and model of morphological Gnathostomata 22 Index 485

characteristics of subphylum 22 Hox genes 242 biological 348 evolution of jaws 241, 256 phylogeny of 90 (n26) and cornmon inductions 343-4 origins of 34 see also Balanoglossus; as continuity of information Gnathostomulida 20, 23, 29 Saccoglossus kowalewski; 342,348 Goethe, J. W. 58 Yunnanozoon Darwin, C. and 336, 349 Goldschmidt, R. 15 (nIl), 308, 379 Heterochronic genes 379 of digits 347-8 see also Hopeful monsters Heterochrony genetic 344-6 Gordian worms, see definition 375 Geoffroy's conception of 59-60, Nematomorpha and developmental processes 336,341 Grainger, R. D. 71 377-9,386 and germ layers 336, 338, 343 Grant, Robert E. 8, 71, 78 ecological context of 379-83 historical 347 Great Chain of Being 7, 15 (n4), and environmental range 381 idealistic morphology and 336, 69 and inductive tissue 347 Griphippus gratus 206-7 interactions 378, 380, 390 Lankester, E. R. and 78, 84 Growth differentiation factor-5 (n8) latent 340-1 and joint formation 265 as pattern 376, 380 ChNen,R.and 73,336,338 Growth factors as process 376 and non-equivalent see also Activin-A; Activin-B; and sexual maturity 376 developmental Bone morphogenetic and small size 381 processes 349-50 proteins; Fibroblast• specific 376 as pattern or process 348-50, and Transforming growth systemic 376 350 (Box 21.2) factors see also Condensations; Haeckel; and regeneration 339-40 Heterochronic genes; see also de Beer, G. R; Lens Haeckel, E. Neoteny; Ontogenetic induction; Serial homology and archetypes 80,82 trajectories; Homoplasy 78,90 (n13), 109 and heterochrony 375 Paedomorphosis; Timing of (nl0), 138 (n5), 351 (n1) and heterotopy 383 development Homunculus 5, 6 and phylogeny 13, 80, 232 Heteroneuralia 28, 29 Hopeful monsters 216 see also Gastraea theory; Heterotopy Hox code 247-8,231 (n3) Recapitulation and developmental processes Hox genes Hagfish 386 and axial patterning 249--51 as craniates, not vertebrates 21, and germ layers 383 in central nervous system 246- 241 and inductive tissue 8,248 relationship to conodonts 27, interaction 384-7, 389 in cephalochordates 243-7 126 and Meckel's cartilage 385-7 chordate allies share retinoic relationship to lampreys 27, and origin of novelties 399, acid-induced 126, 138 (n7), 241 399 regulation 243 Wnt genes and 157 of rodent cheek pouches 384-5 and chordate origins 241-5 see also Agnatha; Bdellostoma Homeosis 147 clusters 226, 242-4 stoutii Homeotic genes combinatorial codes 250--1 Haldane, J. B. S. 12 Antennapedia complex 146-7, disruption 248-9 Halkieriids 49 147, 150, 162 (Box 10.1) evolution of in chordates 241-2 Haller, Albrecht von 4, 8 in arthropod-chordate downstream genes 221 HaUucigenia sparsa 40, 42-3, 44-5, ancestor 244 FGF modifies expression 186 151,231 Bithorax complex 146-7,147, fin ~ limb transition 263 Halocynthia roretzi 159, 171,243, 162 (Box 10.1) fish 245,263 403 in Drosophila 146-8 as guide to homology 246-7 Hardy-Weinberg law 11-12 duplication of 242, 244-6, 398 in hernichordates 242 Harrison, R 186 phyletic distribution 148-50 and limb development 188, Harvey, William 58, 112 in plants 148-50 262-4,263 Hedgehog gene 188 see also Body plans; Homeotic murine Hoxb elicits leg in Heliocidaris erythrogramma 136, mutations Drosophila 242, 345 357-8, 358, 379 Homeotic mutations 102, 147-8 nomenclature 162 (Box 10.1) Heliocidaris tuberculata 357 Homogeny 78, 90 (n13) N-CAM as target 221 Hemicentrotus pulcherrimus 244 Homology overexpression 249 Hemichordata and atavisms 341 phylotypic stages based on 231 features 22, 29 Baer, K. E. von and 336, 337 regeneration of limbs from in Cambrian fauna 46 (Box 21.1) tadpole tails mediated created by Bateson 88 of behaviour 350 (Box 21.2) by 242 486 Index

Hox genes (continued) interactions Lancelets, see Cephalochordates regulation of during Inheritance systems Lankester, E. R. segmentation 221,346 and chromatin structure 118- on Archaeopteryx 255 retinoic acid induces 19,120 (n9) distinguishes homogeny from transformations 162-3,242 cortical 117 homoplasy 78, 90 (n13) shared by arthropods, insects, epigenetic 111, 113-16 and elasmobranch embryos 84 myriapods and genomic imprinting 119, 120 planula theory 90 (n15) onychophorans 54 (n5), (nll) on recapitulation 90 (n24) 188,221 heritable patterns of gene see also Homology 39 in mammals 226 expression 117-19 Latimeria chalumnae 23, 36 (n12) in urochordates 242-3 maternal 116-17 Larvae in vertebrates 245, 247-9 methylation of DNA and 118- adaptations 353-4 zootype based on 229,231 19 developmental mechanisms see also Homeotic genes Innovations, see Key innovations and 234-7 HrPax-37 gene 243,403 Insect wings, evolution of 214-16 evolution of 232-4, 238 (n15- Huxley, J. S. 12 Internal causation 16),353-60 Huxley, T. H. see Functional causation primary 233-4 and evolution as progress 9 secondary 233 as popularizer of science 9 (Box Japanese medaka, see Oryzias set-aside cells 23&-7 1.1) latipes types 128-9, 231-7 and relationships of fishes 32 Jardin du Roi, Paris 61 (Box 4.2), and types of embryogenesis and water babies 6 73 234-7, 235, 236 Hydra 7, 127, 231, 345 Jawless vertebrates volk and 233 Hydractinia symbiolongicarplls 149 see Agnatha; Hagfish; Lampreys La'rvacea Hydromantes 282,292 (n1) Jaw joint evolution 283-4 features 22 Hyolitha 23 Jaws, evolution of 7,240,256, larval evolution 128 255-8 see also Urochordates Ichthyostega 259, 259-60, 262 L-CAM, see Liver cell adhesion Idealistic morphology 58-9, 74 Kangaroo rats 385 molecule Idiocranillm russe/i 381 Keratella lesilldo 301 Lens induction 182,319 (n8) llynassa 236 Key innovations 216-17,222 (n7) and heterochrony 380 Indirect development 128, 233 Darwin and 217 and homology 340, 343, 349 Induction Geoffroy and 60 temperature and 380 of annular ligament 184 in morphology 98, 273 Lepidosiren paradoxa 36 (n 12) of balancers 290-2 Kielmeyer, C. F. 10, 72, 89 (n4) Life history stages of bone 180-1,195 (n9) Killifish, see Fundulus heteroclitus conserved embryonic 129- of cartilage 198, 386 Kimberella quadrata 24,36 (n6), 231 35 of cement glands 355, 360 (n8) Kingdoms 17-18,18,18,24,35 metazoan 127-9 competence 160, 169,360 (n9) (n1) Limb development of cornea 182 Hox gene conservation across avian 184, 185, 184-9 double assurance 109 (n13), 108 FGF-2 and 185-6 181,195 (n11) see a/so Animal kingdom FGF-4 and 187 heterochrony and 378, 3S0, 390 Kinorhyncha 20,29 Hox genes and 262-4 (nS) Kovalevsky, A. O. 85, 85, 87, 90 mutants 188-9, 195 (n16) of kidnevs 193, 193-4 (n22) patterning 264-5 inhibition by neural crest Limb fields 186 193 Lacerta 97, 382 Limbs from fins 258-64 of lens 182,182, 195 (n14) Lamellibrachia 23 Limnaea of Meckel's cartilage 386 Lampetra jluviatilis 245 adaptation to wave action 313- of mesoderm 131, 157, 155-9 Lampetra japonica 258 14 of neural crest 171 Lampreys behaviour modified 314, 317 of neural ectoderm 159-63 engrai/ed gene 258 and genetic assimilation 313- of otic capsule 184, 200 induction of visceral arch 14,317,319 (nlO) of otic vesicle 183 cartilages 386 lin genes 379 primary embryonic 159-60, 239 relationship to hagfishes 22, 27, Liver cell adhesion molecule 179 properties of 160-1 126, 138 (n7), 241 Lobe-finned fish 32 of teeth 189-93 see also Lampetra jluviatilis; see also Sarcopterygians types of 299-300 Lampetra japonica; Lobopodans 43, 221 see a/so Epithelial-mesenchymal Petromyzon marin us Loligo pea Iii 368 Index 487

Loricifera 18, 20, 23, 29 genetic basis of 154--9, 157 Molluscs Loxodonta africana 381 Mesozoa 20, 29 cell determination 226, 235, 236 Lucilia cuprina 208 Metamorphosis phylum definition 21, 29 Lungfish 23, 28, 32, 36 (n12), 126 and bone induction in urodeles timing of fertilization 131 Lyell, Charles 8-9 200 torsion 276-7 Lynx 287 constancy of allometric relations Monerula 80, 82, 391 through 200 Monodelphis 391 (n29) Mackenzia costalis 43 degeneration of balancers Monodelphis domestica 285, 388 Macroevolution 12, 15 (n11), 319 during 290 Morphogenesis (n3) and direct-developing as basic developmental process Mammalian jaw, evolution of 285, amphibians 355 13, 127, 132, 155, 177 386 and direct-developing and differentiation 132 Manx gene in ascidians 359 ascidians 359 as epigenetic process 114 Marrella splendens 40, 40-1, 53 egg size and timing of 314 and epithelial-mesenchymal Mass-specific energy facultative in salamanders 303 interactions 177-8, 181 metabolism 366 genes for competence 353 fields and 231 Maternal constraint 105 larval turnover 128 and fluctuating asymmetry 207 Maternal cytoplasmic control neural-aneural hybrids in gastrulation and 134 and coiling in gastropods 276- ascidians 359 and growth 200-1 7 timing of with different of neural tube 159,161 duration of 116, 116, 132 numbers of moults 370 and ontogenetic of early development 116-17 and tympanic cartilage in repatterning 282 and type 2 embryogenesis 235 urodeles of rotifer spines 300-1 Maternal genome Metazoa 104 and set-aside cells 236-7 and cell lineage in direct Burgess Shale fauna as and symbiosis 302 developers 348 worldwide 39 of teeth 191-2 and determination of primary Cambrian fossil embryonic 40 temperature and 115 body axis 116-17,144-5 complexity and 223-4 Morphospace 50, 50, 52 and directional asymmetry 206 and epigenetic inheritance 215 Morula and dorsalization of embryos (Box 13.1) as ancestral stage 80, 82 158 evolution of multicellularity Msh genes 162 (Box 10.2) ectoderm and endoderm under and 219-21 Msx genes 162 control of 168 (Box 10.2) gastrulation as taxic homology and dentary bone 327 imprinting of 119 of 13 duplicated at origin of maternal genetic effects 328 germ cell determination vertebrates 244 mitochondrial inheritance 129 throughout 141 and limb development 187-9 and models of morphological Haeckel's stages of 79-80, 80 and tooth development 191 change 323 larvae and 84 Muller, F. 78-9, 232, 340 uterine maternal effects 326 origin of 36 (n8,15), 227-37 Multicellularity Matrix-mediated tissue parallels with fungi 104 advantages of 219-20 interactions 180-1 Methanococcus jannaschii 17 evolution of 219-21 see also Epithelial-mesenchymal Methylation of DNA 118-19, 119 and evolution of phyla 138 (n4) interactions (n8),371 origin of 10 Meckel, J. F. 69,89 (n1) Mice, staging 369,370 Mus 125,236 Meckel's cartilage Microevolution 12, 15 (n11) Musca domestica 145 epithelial induction 386, 385--7 Middle ear ossicles 285, 386 Mutations of marsupials 285 Milne-Edwards, H. 66,67 (nlO), of craniofacial region 199-200 Meckel-Serres law 69 70,135 and heterochrony 378-9 Megaevolution 12 Mimetaster 53 Myxozoa 18 Megaptera novaeangliae 290 Model organisms xvi 123-5 Meroistic oocytes 146, 146 and study of evolution 126 Nasal placode 200 Mesenchyme Xenopus as 124--5, 138 (n1), 397 N-CAM, see Neural-cell adhesion features of 105, 178, 177-8 Molecules and morphology 33, 36 molecule from neural crest 167, 170 (Box (n15) Nematoda 20, 29, 226 10.3) Molgula eitrina 379 Nematomorpha 20,29 Mesoderm Molguia oeculta 359 Nemertina 20, 29 Chordin and 157, 157 Molgula oculata 359 Nemoria arizona ria 303,304 induction of amphibian 131, Molguia pacifica 359-60 Neoceratodus forsteri 36 (n12) 155-9,157, 173 (n 3,4) Molgula provisionalis 479 N eop lasia 114 488 Index

Neopilina 23 Notoneuralia 28,29 Parazoa 19,29 Neotenv 377 Notopthalmus viridiscens 205,341 Parthenogenesis 116, 116, 129 see al~o Heterochrony Novelties, see Evolutionary Pax genes 243,344-6 Nephrops 20 novelties Peneus 79 Neurospora 379 Pentadactvllimb 94, 95 Neural-cell adhesion molecule Ontogenetic repatterning 281-4 Pentasto~a 21, 29 embryonic localization 179-80 intensification of function 283-4 Periodization 127 Hox genes regulate 221 new function 284-6 Peripatus 40,42, 131 on neural ectodermal Ontogenetic scaling 376 Peripatus capensis 43 derivatives 167, 179 Ontogeny Peripatus sedgwicki 43 and secondary evolution of 353-60 Petromyzon marinus 245 chondrogenesis 180, 180, and phylogeny 13-14 Pc-G, see Polycomb response 195 (n6), 318 and systematics 337 (Box 21.1) elements Neural crest Onychophora Phalangeal formula 261 (Box 16.1) amphibian fate map 167 in Burgess Shale 40, 42, 42-3 Phallusia mammillata 345 and branchial arches 200, 248 features of phylum 21,29 Pharyngeal jaws 272,271-4,318 and buccal development 198 Hox genes shared with see also Cichlid fishes cell types derived from 106 arthropods 54 (n5) Pharyngula 228-9 evolution of 54 (n6), 240 modes of development 137 Pheidole bicarinata 302, 306 (nll) in fins 258, 261 see also Aysheaia; Opisthopatus Phenocopy 308-9,399 as fourth germ layer 28, 29, 83, cinctipes; Peripatus; Phenotype 166, 168 (Box 10.2), 169 Viviparity canalization and 201-2,310 induction of 164-71, 171 Onychorhynchus mykiss 36 (n12) of the gene 111,117-19 as inhibitor of induction 194, Oogenesis multiple from same genotype 196 (n31) compared with 299-300,309 migration of 135, 165, 360 (n6), spermatogenesis 130 no one-to-one correspondence 386 in insects 146 with genotype 114,321, and tooth development 198, 199 stages and timing of 399 see also Secondary neurulation fertilization 130, 131 redundancy in Hox genes Neural induction 159-63 see also Maternal cytoplasmic and 248, 252-3 Neural keel 343 control; Meroistic oocytes; see also Genetic assimilation; Neurula 134-5 Panoistic oocytes Phenotypic plasticity Neurulation 134-5, 159-63, 343 Opabinia regalis 47,47-9 Phenotypic plasticity see also Central nervous system Ophraella 12, 103 diet-induced 303-5 Nieuwkoop centre 157, 157-8 Opisthopatus cinctipes 136, 137 environmental induction Noggin and mesoderm Oreochromis mossambicus 368 of 313-14 induction 157, 158 Orthology 150 (Box 9.1), 278 (n15) and induction within Norms of reaction 300, 306 (n6), Oryzias latipes 345, 368 species 302-3 313,331 Ossification, modes of 124 (Box plasticity genes and 306 Notochord 8.1) and predator-based and anural ascidian Otx gene 158 induction 300-2 tadpoles 358-60 Owen, Richard Phoronida 18, 21, 29 and ascidian neural and causation 4 Phyla 17-35 induction 243 and homology 73-5 morphological boundaries and comparative vertebrate archetype 74, 89 (n9), of 49-51 gastrulation 354-7 96 number of cell types and 225 and decay experiments 44 and water babies 6 number of genes and 226 and D-V patterning of neural Owenetta 269 origins of 34, 35 tube 192 relationships among 26--35, 29, discovered in amphioxus 85 Paedomorphosis 96 31 discovered in Balanoglossus 88 see also Heterochrony see also listing for individual and epigenetic burden 214 Pair rule genes 144 phyla; Phylotypic stages; and head organizer 156--7 Pander, C. H. 112 Super phyla induction of amphioxus 131 Panderichthys 259, 259 Phylogenetic systematics 13, 15 and kidney induction 193, 194 Panoistic oocytes 146,146 (n12) and primary embryonic Paralogy 150 (Box 9.1), 278 (nI5) Phylogeny induction 159-63,239,240 as gene duplication 150 (Box aims of embryology and 232 shh and 187 9.1), 339 of animals 28 and super phyla Paramecium 117 and cladistics 337 (Box 21.1) Index 489

created by ontogeny 13-15, 389 Premature death mutation, see and dedifferentiation 104 germ layers and 83, 88, 383 Ambystoma mexicanum and homology 339-40 molecular 28, 30-3, 289 Priapulida 18, 21, 29 and preformation 7 and ontogeny 13-14 Primary embryonic in wild and laboratory ontogeny recapitulates 72, 79- induction 159-60, 239 animals 205 81 Proganochelys 269, 269 Regulation of onychophora 137,138 Prokaryotae 17,18 and type 1 embryogenesis 235 of whales 289 Protochorda tes 240 and type 2 embryogenesis 235 Phylotypic period 229 Protoctista 18 Reptile --> mammal transition 284, Phylotypic stages 227-31, 397-8 Protopterus 31, 36 (nI2,13) 286 parallel von Baer's Protostome animals 21-2,28,29, Retinoic acid embryological 30 induces changes in Hox gene archetypes 70 Proximate causation, see Internal expression 162-3, 242 see also Germ-band stages; causation induces limb regeneration from Pharyngula; Zootypes Proximo-distal axis tail stumps 242 Physeter catadon 289 in Drosophila 188 regulation of Hox genes in Pikaia gracilens 43-6, 46, 239 and vertebrate limb chordate allies 243 Placodes 134, 240, 251 (n8), 268 development 184, 263 Rhombomeres 161, 173-4 (nI5) Placozoa 18, 29 in Xenopus 188 Rhyacotriton olympicus 381 Plana ria 127 Pseudocoelomate animals 20-1, Ribbon worms, see Nemertina Plant kingdom 127 28,29 Rodhocetus kasrani 289 Planula larva 223 Psyllophryne didactyla 390 Rotifera 20, 29 Planula theory 90 (n15) Python molurus 102 cyclomorphosis in 300-1 Plastic form and function 106-8, Round worms, see Nematoda 396,398 Quantitative genetics model of Roux, Wilhelm 7,106,172,173 Platyhelminthes 20,29,226 development and (n10) Pleiotropy 115, 201 evolution 117,321-31 Plethodon cinereus 202, 202-3, 205 causal factors 326-9 Saccharomyces cerevisiae 17 Pleurodeles waltl 178,208 (n1) developmental units of 323-4, Saccoglossus kowalewski 242 Pliohippus 288 326,400 Salamanders, phylogeny of 35 Pluteus larva 357 environmental factors 328 Salamandra 202 (n3) Pogonophora 22,23,29 genotype by environment Salmo gairdneri 209 (n16) Poicilia reticulata 302 interactions 328-9, 400 Salps 22 Polycomb response elements epigenetic factors 328 see also Urochordates in Arabadopsis 150, 153 (n10) intrinsic genetic factors 327-8 SAMs, see Substrate adhesion in Drosophila 119, 120 (n10), maternal genetic effects 116-17, molecules Polydactyly 261 (Box 16.1), 262 144, 322, 328 Sarcopterygian fishes 259 Polymorphism Scaleless mutant 378-9 see Cyclomorphosis Radial cleavage 21-2,28,29 Scaphiopus multiplicatus 303, 306 Polyploidy 124 Radial symmetry 19, 28, 29 (nI2) Polypterus 31,36 (n14), 378, 390 Radical fringe, 187-8, 188, 195 (nI8) Schistocerca americana (n9) Rana 355,380 short-germ band Population genetics embryonic stages grasshopper 136, 146, 146 and adaptation 298 Rana esculenta 343, 380 Schmalhausen, 1. 1. and developmental units 328 Rana fusca 343 autonomization 106, 311, 319 evolution as 11-13,399 Rana palustris 201 (n6) and stabilizing selection 312 Rana pereri 205 books on evolutionary Porifera 19,29,226 Rana pipiens 128, 138 (n9), 133, theory 15 (n9), 213-14, 319 Preadaptation 281, 318 200 (n6) Precis coenia 331 Rana sylvatica 200, 313-15, 380 stabilizing selection 218, 311- Preformation Rana temporaria 170 13,319 (n7) as encapsulation 6-7 Ranodon sibiricus 204 and tarsal patterns in evolution as 4-7 Rattus villosissimus 208 urodeles 204 Geoffroy, E. and Ray-finned fishes 32 see also Autonomization; history 312-13 Recapitulation Stabilizing selection nuclear 113 Baer, K. E. von and 107 Sclerotome 163, 164 Ovists 5-6 Agassiz, L. and 76 Scyliorhinus canicula 368 and regeneration 7, 14 (n5) Haeckel, E. and 90 (nI4) Seasonal polymorphism, see Spermists 6 Regeneration 127 Cyclomorphosis 490 Index

Secondary cartilage 180, 197, 317- Sornites see also Secondary neurulation 18 chairy and timing of 372 Talpid3 187-8 Secondary jaw articulations in development of 164 Tardigrada 21,29 birds 318 and Hox code 249-50, 250 Taricha 205, 287 Secondary neurulation 166, 168, see also Sclerotome; Taricha granulosa, 202, 204, 341 171-2,343 Somi tomeres Taricha torosa 193, 193-4, 380 Segmentation Sornitomeres 165 Tarsal bones, patterns in of hindbrain 161-3, 173-4 (n5) Sonic hedgehog gene urodeles 202, 202-5 and homeotic gene and A-P axis 188 Teratology, see Geoffroy, E. expression 147-9 and enamel knot 192 Thermobia domestica 275 in insects 54 (n5), 144-9, 231, and limb development 187 Thomomys bottae 384 275, 319, 397 and sornites 163 Thomomys talpoides 298 and limb patterning 264-5, 265, Speciation 12 Thorius 381, 381 347-8 of amphibians Timing of development 365-7 of mesoderm 372 of cichlid fishes biological time 371 Owen and 74 Species and cell division/cycles 371-2 and vertebrate ancestor 85-8, biological 51, 54 (n8), 348 critical developmental events 90 (n26) evolutionary 51 and 372 of vertebrate skull 74 palaeontological 51 critical periods 372 see also Segmentation genes Spencer, Herbert 11 and inductive decision• Segmentation genes 144-5 evolutionary theories 8-9, 15 making 372 Selection (n8),72 mass-specific metabolism and canalization 104, 201, 310, Spermatogenesis 130 and 367, 373 (n5) 311,317-18 Spiral,leavage 21-2,28,29,36 morphological stages 367-71, and genetic assimilation 309- (n3),276 368 11,314,317,319 Sponges, see Porifera staging tables 367, 368 hierarchical 53, 54 (nll) Spontaneous generation 204 see also Heterochrony stabilizing 218,312,317,319 Stabilizing selection 218, 312, 317, Tissue interactions 199 (n3) 319 (n3) see also Epithelial-mesenchymal see also Genetic assimilation; Staging, see Timing of interactions Stabilizing selection development Tommotion fauna 23 Sepia 64 Stronglyocentrotus 236 Tooth evolution 283 Serial homology 338-9,341-2 Structural reduction Tooth induction Semper, C 85,86 Styela partita 115 developmental events 189-93, Serrate gene 181 Super phyla 198 Serres, E. R. A. 66, 69 arthropod 48-9 enamel knot 191-3,192 see also Meckel-Serres law schemes for 28-9, 36 (n9) genetic control of 190 Sex combs reduced 119, 146-7, zootype and 230-1, 398 growth factors and 191-3 147 Substrate adhesion molecules 179, patterning and EGF 193 shh see Sonic hedgehog 220 Tornarian larva 233 Short gastrulation gene 151-2, 152, Survival of the fittest Torsion in gastropods 276-7 153 (nI2) Symbion pandora 18, 20, 23 Transcriptional regulation 221-2 Sigmodon fulviventer 104 Symbiosis and induction 302 Transitions in animal evolution Simpson, G. G. 12 Symmetry, see Bilateral symmetry; dinosaurs --) birds 265-7 Sinornis santensis 266 Radial Symmetry gastropod torsion 276-7 Sinosauropteryx prima 266 Symonds, J. A. 71 fins --) limbs 238-<:;5 Sipuncula 21, 29 Synapomorphies insect wings 274-<:i Size and heterochrony 381 of animal kingdom 227 jawed --) jawless vertebrates Sminthopsis macroura 174 (n25) developmental units as 330 255-8 Snakes of gastropods 279 (n32) pharyngeal jaws 271-4 jaw joints 283-4 homology as 332 (nI6), 336 scales --) feathers 265-7 loss of limbs in 267 and key innovations 277 turtle shells 269-71 skull 282 neural crest as vertebrate 186 Trematops milleri 204 sog see Short gastrulation gene (Box 10.2) Tribolium castaneum Soma, distinct from germ and time of origin of feature 98 body plan 145-7, 153 (n7) plasm 4, 141-2 meroistic ovary 146 Somatic embryogenesis 141 Tabby mutant 317 Trichoplax adhaerens 18, 19, 90 Somatic inheritance 4 Tail bud development 172, 175 (nI4),102 Somatoplasm, see Soma (n39,40) Trilobites 40 Index 491

Trithorax response element 119, Vestigial tail 172 Xenopus 120 (nlO) Vestiges, see Chambers, Robert caudal neurulation 172 Triton 291, 380 Vestimentifera 18,22,23, 29,35 cement gland 355, 360 (n8) see also Triturus V g-1 157, 158 chordin and 152, 153 (n12) Triturus alpestris 194, 200, 208 Viviparity craniofacial development 208 (n3), 209 (nI2), 389 onychophoran 137 (n3),355 Triturus carnifex 202, 205 vertebrate 136, 306 (n5), 313 dorso-ventral axis 151, 152, Triturus cristatus 204 Volvox 219-20 246 Triturus mannoratus 204, 348 fate map 163,174 (n26), 220-1, Trochophore larva 21-2 Waddington, C. H. 222 (n13) Tullimonstrum gregarium canalization 201-2 maternal cytoplasmic Tunicates 22, see also Urochordates and epigenetics 11, 119 (n4), control 116 Turnagra capensis 290 201 mesoderm formation 156--9, Turtle shell, see Carapace genetic assimilation 106, 307- 157 Turtles 13 neural crest induction 167, 169, evolution 269,269-70 see also Canalization; Genetic 175 (n28) see also Chelonia midas; Chelydra; assimilation Pax-6 and 351 (n13) Proganochelys Walcott, C. D. 39,53 (n3) skeletal novelties 222 (n6), 381 Type concept, see Unity of type Weismann, August 142, 152 (n1) tadpole 98 Whales, loss of hind limbs 289- Vg-l and, 154, 206, 209 (n15) Ubx, see Ultrabithorax 90 Xbap gene and 200 Ultimate causation, see External Whitman, C. O. 13, 15 (n2) zoo type and 229-30 causation Williston's rule 14 Xenopus laevis ultrabithorax 147, 146--7, 244 Wilson, E. B. cleavage pattern 124 regulated by engrailed 275 cell biology 94, 113, 383 egg 354,355 Unenlagia comahuensis 266, 278 and homology 337,350,350 lens induction 372 (nI9) (n4) staging 368 Uniramia 40, 54 (n4) Wingless gene thyroid axis 360 (n5) Unity of plan, see Unity of type and D-V axis 188 type 2 embryogenesis 235, Unity of type 57-61,64 Wingless mutant 184 236 Unterbaupliine 97-8 Wiwaxia corrugata 47, 48, 49 see also Model organisms see also Baupliine related to halkieriids 48 Xerophytic plants 314 Urbilateria 231, 237 (nI2) related to polychaetes 48 XVent-2 gene in Drosophila 160 Urmollusk 96 Wnt genes Xwnt genes 158 Urochordates and ancestral metazoans 257 basic plan 22, 27, 29, 240 and mesoderm induction 157, Yunnanozoon lividum 46 cell determination in 226 158 Hox genes and 242-3 and limb development 186--7 Zebrafish, see Danio rerio Ula stansburiana 209 (nI6) and neural crest induction 164 Zoea, see Crustacea Wolff, C. F. and epigenesis 112 Zone of polarizing activity 184, Velvet worms, see Onychophora Woodger, J. H. 185,187 Vendobionta 24 influence on biology 93-5, 336 Zootypes 229-31,397 Vertebrates and pentadactyl limb 95 ZP A see Zone of polarizing ancestors 84-8 see also Baupliine activity axial patterning 249-51 Wright, Sewall 12, 115, 201 Zygote 129-32 Hox code 242-8 Zygotic genome 132 origins 245 X chromosome inactivation 118