Skip to main content Accessibility help
×
Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-28T18:30:15.863Z Has data issue: false hasContentIssue false

12 - A molecular–morphological study of a peculiar limb morphology: the development and evolution of the mole's ‘thumb’

Published online by Cambridge University Press:  05 November 2012

Robert J. Asher
Affiliation:
University of Cambridge
Johannes Müller
Affiliation:
Museum für Naturkunde; Humboldt Universität zu Berlin
Get access

Summary

Introduction

Few areas of evolutionary investigation have benefited so much from the integration of molecular and morphological studies as that of the evolution of limbs (e.g. Shubin et al. 2009). Much effort has been concentrated on understanding the transition from ‘fins to limbs’ (Westoll 1943; Coates 1995; Shubin 1995; Shubin et al. 1997, 2004, 2006; Coates et al. 2002; Johanson et al. 2007; Larsson 2007) – for a recent summary of different aspects see Hall (2007) – but also major advances have been made concerning the origin and development of particularly specialized limbs such as those of bats (Sears et al. 2006; Sears 2008), whales (Thewissen et al. 2006), or their absence in snakes (Cohn and Tickle 1999). In fact, tetrapod limbs exhibit a stunning morphological diversity, reflecting their recruitment for a wide variety of functions ranging from walking to watch-making, often deployed as multipurpose structures serving in locomotion and support, personal hygiene, fighting, mating, manipulation and communication.

The reconstructed ground pattern of extant tetrapods may be viewed as a limb with a proximal stylopod (humeral/femoral region), a zeugopod (radial and ulnar/tibial and fibular region) and a distal, pentadactylous autopod (carpal/tarsal region), which contains the proximal mesopodium (wrist and ankle bones) and the terminal acropodium (the digits). With the notable exception of limbless tetrapods, most tetrapod limbs conservatively retain this pattern (Goodwin and Trainor 1983; Holder 1983). Based on these components, the diversity of skeletal morphology in tetrapod limbs is generated largely by differential growth and proportional changes of the common elements. Regarding the acropodia, hypodactyly, hyperphalangy and modifications of branching patterns involve various developmental mechanisms (Motani 1999; Hamrick 2001b, 2002; Richardson and Oelschläger 2002; Fedak and Hall 2004; Sears et al. 2007; Rolian 2008; Weisbecker and Nilsson 2008; Cooper and Dawson 2009).

Type
Chapter
Information
From Clone to Bone
The Synergy of Morphological and Molecular Tools in Palaeobiology
, pp. 301 - 327
Publisher: Cambridge University Press
Print publication year: 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abouheif, E. 1997 Developmental genetics and homology: a hierarchical approachTrends in Ecology and Evolution 12 405CrossRefGoogle ScholarPubMed
Alberch, P. 1985 Developmental constraints: why St. Bernards often have an extra digit and poodles never doAmerican Naturalist 126 430CrossRefGoogle Scholar
Asher, R.Bennett, N.Lehmann, T. 2009 The new framework for understanding placental mammal evolutionBioEssays 31 853CrossRefGoogle ScholarPubMed
Bardeleben, K. 1885 Zur Morphologie des Hand-und FussskeletsJenaische Zeitschrift für Naturwissenschaften 19 84Google Scholar
Bardeleben, K. 1890 Über die Hand-und Fuß-Muskeln der Säugetiere, besonders die des Praepollex (Praehallux) und PostminimusAnatomischer Anzeiger 5 435Google Scholar
Barrionuevo, F.Zurita, F.Burgos, M.Jiménez, R. 2004 Developmental stages and growth rate of the mole (Insectivora, Mammalia)Journal of Mammalogy 85 120CrossRefGoogle Scholar
Bensoussan-Trigano, V.Lallemand, Y.Saint Cloment, C.Robert, B. 2011 and in limb mesenchyme modulate digit number and identityDevelopmental Dynamics 240 1190CrossRefGoogle ScholarPubMed
Blanco, M.Misof, B.Wagner, G. 1998 Heterochronic differences of Hoxa-11 expression in fore- and hind limb development: evidence for lower limb identity of the anuran ankle bonesDevelopment Genes and Evolution 208 175CrossRefGoogle ScholarPubMed
Boisvert, C.Mark-Kurik, E.Ahlberg, P. 2008 The pectoral fin of and the origin of digitsNature 456 636CrossRefGoogle ScholarPubMed
Bolker, J. A. 1995 Model systems in developmental biologyBioEssays 17 451CrossRefGoogle ScholarPubMed
Braus, H. 1906 Die Entwickelung der Form der Extremitäten und des ExtremitätenskelettsHandbuch der vergleichenden und experimentellen Entwickelungslehre der Wirbeltiere, Dritter BandHertwig, O.Jena, GermanyVerlag von Gustav Fischer167Google Scholar
Burke, A. C.Alberch, P. 1985 The development and homology of the chelonian carpus and tarsusJournal of Morphology 186 119CrossRefGoogle Scholar
Burke, A. C.Feduccia, A. 1997 Developmental patterns and the identification of homologies in the avian handScience 278 666CrossRefGoogle Scholar
Buscalioni, A. D.Ortega, F.Rasskin-Gutman, D.Pérez-Moreno, B. P. 1997 Loss of carpal elements in crocodilian limb evolution: morphogenetic model corroborated by palaeobiological dataBiological Journal of the Linnean Society 62 133CrossRefGoogle Scholar
Camardi, G. 2001 Richard Owen, morphology and evolutionJournal of the History of Biology 34 481CrossRefGoogle Scholar
Carmona, F. D.Motokawa, M.Tokita, M. 2008 The evolution of female mole ovotestes evidences high plasticity of mammalian gonad developmentJournal of Experimental Zoology–Molecular and Developmental Evolution 310B 259CrossRefGoogle Scholar
Carmona, F. D.Lupiáñez, D. G.Real, F. M. 2009 Sox9 is not required for the cellular events of testicular organogenesis in XX mole ovotestesJournal of Experimental Zoology–Molecular and Developmental Evolution) 312B 734CrossRefGoogle Scholar
Chimal-Monroy, J.Rodriguez-Leon, J.Montero, J. A. 2003 Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signalingDevelopmental Biology 257 292CrossRefGoogle ScholarPubMed
Coates, M. I. 1995 Fish fins or tetrapod limbs – a simple twist of fate?Current Biology 5 844CrossRefGoogle ScholarPubMed
Coates, M. I.Clack, J. A. 1990 Polydactyly in the earliest known tetrapod limbsNature 347 66CrossRefGoogle Scholar
Coates, M.Jeffery, J.Ruta, M. 2002 Fins to limbs: what the fossils sayEvolution and Development 4 390CrossRefGoogle ScholarPubMed
Cohn, M. J.Bright, P. E. 1999 Molecular control of vertebrate limb development, evolution and congenital malformationsCell and Tissue Research 296 3CrossRefGoogle ScholarPubMed
Cohn, M. J.Tickle, C. 1999 Developmental basis of limblessness and axial patterning in snakesNature 399 474CrossRefGoogle ScholarPubMed
Cooper, L. N.Dawson, S. D. 2009 The trouble with flippers: a report on the prevalence of digital anomalies in CetaceaZoological Journal of the Linnean Society 155 722CrossRefGoogle Scholar
Daeschler, E.Shubin, N. 1997 Fish with fingers?Nature 391Google Scholar
Dahn, R. D.Fallon, J. F. 2000 Interdigital regulation of digit identity and homeotic transformation by modulated BMP signalingScience 289 438CrossRefGoogle ScholarPubMed
Dahn, R. D.Davis, M. C.Pappano, W. N.Shubin, N. H. 2007 Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterningNature 445 311CrossRefGoogle ScholarPubMed
Davidson, D. 1995 The function and evolution of Msx genes: pointers and paradoxesTrends in Genetics 11 405CrossRefGoogle ScholarPubMed
Delfino, M.Sánchez-Villagra, M. R. 2010 A survey of the rock record of reptilian ontogenySeminars in Cell and Developmental Biology 21 432CrossRefGoogle ScholarPubMed
Delfino, M.Fritz, U.Sánchez-Villagra, M. R. 2010 Evolutionary and developmental aspects of phalangeal formula variation in pig-nose and soft-shelled turtles (Carettochelyidae and Trionychidae)Organisms Diversity and Evolution 10 69CrossRefGoogle Scholar
Deschamps, J. 2008 Tailored Hox gene transcription and the making of the thumbGenes and Development 22 293CrossRefGoogle ScholarPubMed
Dingerkus, G.Uhler, L. D. 1977 Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilageStain Technology 52 229CrossRefGoogle ScholarPubMed
Donoghue, P. C. J.Graham, A.Kelsh, R. N. 2008 The origin and evolution of the neural crestBioEssays 30 530CrossRefGoogle ScholarPubMed
Drossopoulou, G.Lewis, K. E.Sanz-Ezquerro, J. J. 2000 A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signaling and Bmp signalingDevelopment 127 1337Google Scholar
Duboule, D. 2010 The evo-devo cometEMBO reports 11CrossRefGoogle ScholarPubMed
Edwards, L. F. 1937 Morphology of the forelimb of the mole (, L.) in relation to its fossorial habitsOhio Journal of Science 37 20Google Scholar
Emery, C. 1890 Zur Morphologie des Hand-und FußskelettsAnatomischer Anzeiger 5 283Google Scholar
Endo, H.Yamagiwa, D.Hayashi, Y. 1999 Role of the giant panda's ‘pseudo-thumb’Nature 397 309CrossRefGoogle Scholar
Fabrezi, M. 1993 The anuran tarsusAlytes 11 47Google Scholar
Fabrezi, M. 2001 A survey of prepollex and prehallux variation in anuran limbsZoological Journal of the Linnean Society 131 227CrossRefGoogle Scholar
Fabrezi, M.Alberch, P. 1996 The carpal elements of anuransHerpetologica 52 188Google Scholar
Fabrezi, M.Barg, M. 2001 Patterns of carpal development among anuran amphibiansJournal of Morphology 249 210CrossRefGoogle ScholarPubMed
Fedak, T. J.Hall, B. K. 2004 Perspectives on hyperphalangy: patterns and processesJournal of Anatomy 204 151CrossRefGoogle ScholarPubMed
Fröbisch, N. B. 2008 Ossification patterns in the tetrapod limb – conservation and divergence from morphogenetic eventsBiological Reviews of the Cambridge Philosophical Society 83 571CrossRefGoogle ScholarPubMed
Fröbisch, N. B.Carroll, R. L.Schoch, R. R. 2007 Limb ossification in the Paleozoic branchiosaurid (Temnospondyli) and the early evolution of preaxial dominance in tetrapod limb developmentEvolution and Development 9 69CrossRefGoogle ScholarPubMed
Galis, F.Alphen, J. J. M. vanMetz, J. A. J. 2001 Why five fingers? Evolutionary constraints on digit numbersTrends in Ecology and Evolution 16 637CrossRefGoogle Scholar
Galis, F.Alphen, J. J. M. vanMetz, J. A. J. 2002 Digit reduction: via repatterning or developmental arrest?Evolution and Development 4 249CrossRefGoogle ScholarPubMed
Galis, F.Kundrát, M.Sinervo, B. 2003 An old controversy solved: bird embryos have five fingersTrends in Ecology and Evolution 18 7CrossRefGoogle Scholar
Gañan, Y.Macias, D.Hurle, J. M. 1994 Pattern regulation in the chick autopodium at advanced stages of embryonic developmentDevelopmental Dynamics 199 64CrossRefGoogle ScholarPubMed
Gañan, Y.Macias, D.Basco, R. D.Merino, R.Hurle, J. M. 1998 Morphological diversity of the avian foot is related with the pattern of Msx gene expression in the developing autopodDevelopmental Biology 196 33CrossRefGoogle ScholarPubMed
Gegenbaur, C. 1898 Vergleichende Anatomie der Wirbelthiere mit Berücksichtigung der Wirbellosen. Band 1: Einleitung, Integument, Skeletsystem, Muskelsystem, Nervensystem und SinnesorganeLeipzig, GermanyVerlag von Wilhelm EngelmannGoogle Scholar
Gilbert, S. F. 2003 The morphogenesis of evolutionary developmental biologyInternational Journal of Developmental Biology 47 467Google ScholarPubMed
Goodwin, B. C.Trainor, L. E. H. 1983 The ontogeny and phylogeny of the pentadactyl limbDevelopment and EvolutionGoodwin, B.Holder, N.Wylie, C. C.Cambridge, UKCambridge University Press75Google Scholar
Hall, B. 2003 Unlocking the black box between genotype and phenotype: cell condensations as morphogenetic (modular) unitsBiology and Philosophy 18 219CrossRefGoogle Scholar
Hall, B 2005 Bones and Cartilage: Developmental and Evolutionary Skeletal BiologyAmsterdam, NetherlandsElsevier Academic PressGoogle Scholar
Hall, B. 2007 Fins into LimbsChicago, ILUniversity of Chicago PressGoogle Scholar
Hamrick, M. W. 2001 Development and evolution of the mammalian limb: adaptive diversification of nails, hooves, and clawsEvolution and Development 3 3555CrossRefGoogle ScholarPubMed
Hamrick, M. W. 2001 Primate origins: evolutionary change in digital ray patterning and segmentationJournal of Human Evolution 40 339CrossRefGoogle ScholarPubMed
Hamrick, M. W. 2002 Developmental mechanisms of digit reductionEvolution and Development 4 247CrossRefGoogle ScholarPubMed
Hamrick, M. W. 2003 Evolution and development of mammalian limb integumentary structuresJournal of Experimental Zoology–Molecular and Developmental Evolution 298B 152CrossRefGoogle Scholar
Hanken, J. 1993 Model systems versus outgroups: alternative approaches to the study of head development and evolutionAmerican Zoologist 33 448CrossRefGoogle Scholar
Harfe, B. D.Scherz, P. J.Nissim, S. 2004 Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identitiesCell 118 517CrossRefGoogle ScholarPubMed
Hentschel, H. G. E.Glimm, T.Glazier, J. A.Newman, S. A. 2004 Dynamical mechanisms for skeletal pattern formation in the vertebrate limbProceedings of the Royal Society of London B 271 1713CrossRefGoogle ScholarPubMed
Hinchliffe, J. 1989 Evolutionary aspects of the developmental mechanisms underlying the patterning of the pentadactyl limb skeleton in birds and other tetrapodsFortschritte der Zoologie 35 226Google Scholar
Hinchliffe, J. R 2002 Developmental basis of limb evolutionInternational Journal of Developmental Biology 46 835Google ScholarPubMed
Hinchliffe, J.Griffiths, P. 1983 The prechondrogenic patterns in tetrapod limb development and their phylogenetic significanceDevelopment and EvolutionGoodwin, B.Holder, N.Wylie, C. C.Cambridge, UKCambridge University Press99Google Scholar
Holder, N. 1983 The vertebrate limb: patterns and constraints in development and evolutionDevelopment and EvolutionGoodwin, B.Holder, N.Wylie, C. C.Cambridge, UKCambridge University Press399Google Scholar
Holmgren, N. 1933 On the origin of the tetrapod limbActa Zoologica 14 185CrossRefGoogle Scholar
Holmgren, N. 1952 An embryological analysis of the mammalian carpus and its bearing upon the question of the origin of the tetrapod limbActa Zoologica 33 1CrossRefGoogle Scholar
Hugi, J.Mitgutsch, C.Sánchez-Villagra, M. R. 2010 Chondrogenic and ossification patterns and sequences in White's skink (Scincidae, Reptilia)Zoosystematics and Evolution 86 21CrossRefGoogle Scholar
Izpisúa-Belmonte, J. C.Ede, D. A.Tickle, C.Duboule, D. 1992 The mis-expression of posterior Hox-4 genes in talpid (ta3) mutant wings correlates with the absence of anteroposterior polarityDevelopment 114 959Google ScholarPubMed
James, W. H. 1998 Hypothesis: one cause of polydactylyJournal of Theoretical Biology 192 1CrossRefGoogle ScholarPubMed
Janies, D.de Salle, R. 1999 Development, evolution, and corroborationAnatomical Record (New Anatomist) 257 63.0.CO;2-I>CrossRefGoogle ScholarPubMed
Jenner, R. A.Wills, M. A. 2007 The choice of model organisms in evo-devoNature Reviews Genetics 8 311CrossRefGoogle ScholarPubMed
Jiménez, R.Burgos, M.Sánchez, A. 1993 Fertile females of the mole are phenotypic intersexes with ovotestesDevelopment 118 1303Google ScholarPubMed
Johanson, Z.Joss, J. M. P.Sutija, M.Boisvert, C.Ahlberg, P. E. 2007 Fish fingers: digit homologues in sarcopterygian fish finsJournal of Experimental Zoology–Molecular and Developmental Evolution 308B 757CrossRefGoogle Scholar
Kellogg, E. A.Shaffer, H. B. 1993 Model organisms in evolutionary studiesSystematic Biology 42 409CrossRefGoogle Scholar
Kindahl, M. 1942 Einige Mitteilungen über die Entwicklung der Hand und des Fußes bei LZeitschrift für mikroskopisch-anatomische Forschung 52 267Google Scholar
Kley, N.Kearney, M. 2007 Adaptations for digging and burrowingFins into Limbs: Evolution, Development, and TransformationHall, B.Chicago, ILUniversity of Chicago Press284Google Scholar
Kundrát, M. 2009 Primary chondrification foci in the wing basipodium of with comments on interpretation of autopodial elements in Crocodilia and AvesJournal of Experimental Zoology–Molecular and Developmental Evolution 312B 30CrossRefGoogle Scholar
Lallemand, Y.Nicola, M.Ramos, C. 2005 Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb developmentDevelopment 132 3003CrossRefGoogle ScholarPubMed
Lallemand, Y.Bensoussan, V.Saint Cloment, C.Robert, B. 2009 Msx genes are important apoptosis effectors downstream of the Shh/Gli3 pathway in the limbDevelopmental Biology 331 189CrossRefGoogle ScholarPubMed
Larsson, H. 2007 MODEs of developmental evolution: an example with the origin and definition of the autopodiumMajor Transitions in Vertebrate EvolutionAnderson, J.Sues, H.Bloomington, INIndiana University Press150Google Scholar
Larsson, H. C. E.Wagner, G. P. 2002 Pentadactyl ground state of the avian wingJournal of Experimental Zoology–Molecular and Developmental Evolution 294 146CrossRefGoogle ScholarPubMed
Larsson, H. C. E.Wagner, G. P. 2003 Old morphologies misinterpretedTrends in Ecology and Evolution 18CrossRefGoogle Scholar
Larsson, H. C. E.Heppleston, A. C.Elsey, R. M. 2010 Pentadactyl ground state of the manus of and insights into the evolution of digital reduction in ArchosauriaJournal of Experimental Zoology–Molecular and Developmental Evolution 314B 571CrossRefGoogle Scholar
Le Minor, J. 1994 The sesamoid bone of musculus abductor pollicis longus (os radiale externum or prepollex) in PrimatesActa Anatomica 150 227CrossRefGoogle Scholar
Leal, F.Tarazona, O. A.Ramírez-Pinilla, M. P. 2010 Limb development in the gekkonid lizard : a reconsideration of homology in the lizard carpus and tarsusJournal of Morphology 271 1328CrossRefGoogle ScholarPubMed
Lebedev, O.Coates, M. 1995 The postcranial skeleton of the Devonian tetrapod LebedevZoological Journal of the Linnean Society 114 307CrossRefGoogle Scholar
Lefebvre, V.Smits, P. 2005 Transcriptional control of chondrocyte fate and differentiationBirth Defects Research (Part C) 75 200CrossRefGoogle Scholar
Lefebvre, V.Dumitriu, B.Penzo-Méndez, A.Han, Y.Pallavi, B. 2007 Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factorsInternational Journal of Biochemistry and Cell Biology 39 2195CrossRefGoogle ScholarPubMed
Lettice, L. A.Heaney, S. J.Purdie, L. A. 2003 A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactylyHuman Molecular Genetics 12 1725CrossRefGoogle ScholarPubMed
Lewis, O. 1964 The homologies of the mammalian tarsal bonesJournal of Anatomy 98 195Google ScholarPubMed
Litingtung, Y.Dahn, R. D.Li, Y.Fallon, J. F.Chiang, C. 2002 Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identityNature 418 979CrossRefGoogle ScholarPubMed
Lunde, D. P.Schutt, W. A. 1999 The peculiar carpal tubercles of male and (Didelphidae: Didelphinae)Mammalia 63 495CrossRefGoogle Scholar
Mathews, L. 1935 The oestrous cycle and intersexuality in the female mole ( Linn)Proceedings of the Royal Society of London 2 347Google Scholar
McGlinn, E.van Bueren, K. L.Fiorenza, S. 2005 and act downstream of Gli3 in vertebrate limb developmentMechanisms of Development 122 1218CrossRefGoogle ScholarPubMed
Metscher, B. D.Ahlberg, P. E. 1999 Zebrafish in context: uses of a laboratory model in comparative studiesDevelopmental Biology 210 1CrossRefGoogle ScholarPubMed
Milinkovitch, M.Tzika, A. 2007 Escaping the mouse trap: the selection of new evo-devo model speciesJournal of Experimental Zoology–Molecular and Developmental Evolution 308B 337CrossRefGoogle Scholar
Mitgutsch, C. 2003 On Carl Gegenbaur's theory on head metamerism and the selection of taxa for comparisonsTheory in Biosciences 122 204Google Scholar
Mitgutsch, C.Richardson, M. K.Jiménez, R. 2012 Circumventing the polydactyly ‘constraint’: the mole's ‘thumb’Biology Letters 8 74CrossRefGoogle Scholar
Montavon, T.Le Garrec, J. F.Kerszberg, M.Duboule, D. 2008 Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbnessGenes and Development 22 346CrossRefGoogle ScholarPubMed
Montero, J. A.Lorda-Diez, C. I.Gañan, Y.Macias, D.Hurle, J. M. 2008 Activin/TGFβ and BMP crosstalk determines digit chondrogenesisDevelopmental Biology 321 343CrossRefGoogle ScholarPubMed
Motani, R. 1999 On the evolution and homologies of ichthyopterygian forefinsJournal of Vertebrate Paleontology 19 28CrossRefGoogle Scholar
Müller, G. B. 2007 Evo-devo: extending the evolutionary synthesisNature Reviews Genetics 8 943CrossRefGoogle ScholarPubMed
Ortega-Ortiz, J. G.Villa-Ramírez, B.Gersenowies, J. R. 2000 Polydactyly and other features of the manus of the vaquita, Marine Mammal Science 16 277CrossRefGoogle Scholar
Oster, G. F.Murray, J. D.Harris, A. K. 1983 Mechanical aspects of mesenchymal morphogenesisJournal of Embryology and Experimental Morphology 78 83Google ScholarPubMed
Oster, G. F.Shubin, N.Murray, J. D.Alberch, P. 1988 Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogenyEvolution 42 862CrossRefGoogle ScholarPubMed
Peterson, K. J.Summons, R. E.Donoghue, P. C. J. 2007 Molecular palaeobiologyPalaeontology 50 775CrossRefGoogle Scholar
Pritchett, J. 1984 The incidence of fabellae in osteoarthrosis of the kneeJournal of Bone and Joint Surgery 66 1379CrossRefGoogle ScholarPubMed
Prochel, J. 2006 Early skeletal development in , the common European moleZoological Science 23 427CrossRefGoogle ScholarPubMed
Prochel, J.Sánchez-Villagra, M. 2003 Carpal ontogeny in and (Marsupialia)Zoology 106 73CrossRefGoogle Scholar
Prochel, J.Vogel, P.Sánchez-Villagra, M. 2004 Hand development and sequence of ossification in the forelimb of the European shrew (Soricidae) and comparisons across therian mammalsJournal of Anatomy 205 99CrossRefGoogle ScholarPubMed
Reed, C. A. 1951 Locomotion and appendicular anatomy in three soricoid insectivoresAmerican Midland Naturalist 45 513CrossRefGoogle Scholar
Richardson, M.Jeffery, J.Tabin, C J. 2004 Proximodistal patterning of the limb: insights from evolutionary morphologyEvolution and Development 6 1CrossRefGoogle ScholarPubMed
Richardson, M. K.Oelschläger, H. H. A. 2002 Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipperEvolution and Development 4 435CrossRefGoogle ScholarPubMed
Richardson, M. K.Gobes, S. M.van Leeuwen, A. C. 2009 Heterochrony in limb evolution: developmental mechanisms and natural selectionJournal of Experimental Zoology–Molecular Development and Evolutio 312B 639CrossRefGoogle Scholar
Rieppel, O. 1993 Studies on skeleton formation in reptiles. II. (Squamata: Chamaeleoninae), with comments on the homology of carpal and tarsal bonesHerpetologica 49 66Google Scholar
Rieppel, O. 1993 Studies on skeleton formation in reptiles: patterns of ossification in the skeleton of (Reptilia, Testudines)Journal of Zoology 231 487CrossRefGoogle Scholar
Rolian, C. 2008 Developmental basis of limb length in rodents: evidence for multiple divisions of labor in mechanisms of endochondral bone growthEvolution and Development 10 15CrossRefGoogle ScholarPubMed
Romer, A. S. 1956 Osteology of the ReptilesChicago, ILChicago University PressGoogle Scholar
Roush, W. 1996 Zebrafish embryology builds better model vertebrateScience 272CrossRefGoogle ScholarPubMed
Roybal, P. G.Wu, N. L.Sun, J. 2010 Inactivation of Msx1 and Msx2 in neural crest reveals an unexpected role in suppressing heterotopic bone formation in the headDevelopmental Biology 343 28CrossRefGoogle ScholarPubMed
Sahar, D.Longaker, M.Quarto, N. 2005 Sox9 neural crest determinant gene controls patterning and closure of the posterior frontal cranial sutureDevelopmental Biology 280 344CrossRefGoogle ScholarPubMed
Sánchez, A.Bullejos, M.Burgos, M. 1996 Females of four mole species of genus (Insectivora, Mammalia) are true hermaphrodites with ovotestesMolecular Reproduction and Development 44 2893.0.CO;2-I>CrossRefGoogle ScholarPubMed
Sánchez-Villagra, M. R.Menke, P. R. 2005 The mole's thumb – evolution of the hand skeleton in talpids (Mammalia)Zoology 108 3CrossRefGoogle Scholar
Sánchez-Villagra, M. R.Horovitz, I.Motokawa, M. 2006 A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationshipsCladistics 22 59CrossRefGoogle Scholar
Sánchez-Villagra, M. R.Mitgutsch, C.Nagashima, H.Kuratani, S. 2007 Autopodial development in the sea turtles and Zoological Science 24 257CrossRefGoogle Scholar
Sarin, V.Erickson, G.Giori, N.Bergman, A.Carter, D. 1999 Coincident development of sesamoid bones and clues to their evolutionAnatomical Record (New Anatomist) 257 1743.0.CO;2-O>CrossRefGoogle ScholarPubMed
Schmidt-Ehrenberg, E. 1942 Die Embryogenese des Extremitätenskelettes der SäugetiereRevue Suisse de Zoologie 49 33Google Scholar
Scholtz, G. 2005 Homology and ontogeny: pattern and process in comparative developmental biologyTheory in Biosciences 124 121CrossRefGoogle ScholarPubMed
Sears, K. 2008 Molecular determinants of bat wing developmentCells, Tissues, Organs 187 6CrossRefGoogle ScholarPubMed
Sears, K. E.Behringer, R. R.Rasweiler, J. J. T.Niswander, L. A. 2006 Development of bat flight: morphologic and molecular evolution of bat wing digitsProceedings of the National Academy of Sciences of the United States of America 103 6581CrossRefGoogle ScholarPubMed
Sears, K. E.Behringer, R. R.Rasweiler, J. J.Niswander, L. A 2007 The evolutionary and developmental basis of parallel reduction in mammalian zeugopod elementsAmerican Naturalist 169 105CrossRefGoogle ScholarPubMed
Shubin, N. 1995 The evolution of paired fins and the origin of tetrapod limbsEvolutionary Biology 28 39Google Scholar
Shubin, N. H.Alberch, P. 1986 A morphogenetic approach to the origin and basic organization of the tetrapod limbEvolutionary Biology 20 319Google Scholar
Shubin, N.Wake, D. B.Crawford, A. J. 1995 Morphological variation in the limbs of (Caudata: Salamandridae): evolutionary and phylogenetic implicationsEvolution 49 874CrossRefGoogle ScholarPubMed
Shubin, N.Tabin, C.Carroll, S. 1997 Fossils, genes and the evolution of animal limbsNature 388 639CrossRefGoogle ScholarPubMed
Shubin, N. H.Daeschler, E. B.Coates, M. I. 2004 The early evolution of the tetrapod humerusScience 304 90CrossRefGoogle ScholarPubMed
Shubin, N. H.Daeschler, E. B.Jenkins, F. A. 2006 The pectoral fin of and the origin of the tetrapod limbNature 440 764CrossRefGoogle ScholarPubMed
Shubin, N.Tabin, CCarroll, S. 2009 Deep homology and the origins of evolutionary noveltyNature 457 818CrossRefGoogle ScholarPubMed
Slack, J. M. W.Holland, P. W. H.Graham, C. F. 1993 The zootype and the phylotypic stageNature 361 490CrossRefGoogle ScholarPubMed
Stafford, B. J.Thorington, R. W. 1998 Carpal development and morphology in archontan mammalsJournal of Morphology 235 1353.0.CO;2-8>CrossRefGoogle ScholarPubMed
Starck, D. 1979 Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage. Band 2: Das Skeletsystem. Allgemeines, Skeletsubstanzen, Skelet der Wirbeltiere einschließlich LokomotionstypenBerlinSpringer-VerlagCrossRefGoogle Scholar
Svensson, M. E. 2004 Homology and homocracy revisited: gene expression patterns and hypotheses of homologyDevelopment Genes and Evolution 214 418CrossRefGoogle ScholarPubMed
Tabin, C. J. 1992 Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbsDevelopment 116 289Google ScholarPubMed
Tamura, K.Nomura, N.Seki, R.Yonei-Tamura, S.Yokoyama, H. 2011 Embryological evidence identifies wing digits in birds as digits 1, 2, and 3Science 331 753CrossRefGoogle Scholar
Thewissen, J. G. M.Cohn, M. J.Stevens, L. S. 2006 Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplanProceedings of the National Academy of Sciences of the United States of America 103 8414CrossRefGoogle ScholarPubMed
Thorington, R. W.Stafford, B. J. 2001 Homologies of the carpal bones in flying squirrels (Pteromyinae): a reviewMammal Study 26 61CrossRefGoogle Scholar
Tokita, M.Iwai, N. 2010 Development of the pseudothumb in frogsBiology Letters 6 517CrossRefGoogle ScholarPubMed
Vargas, A. O.Fallon, J. F. 2005 Birds have dinosaur wings: the molecular evidenceJournal of Experimental Zoology–Molecular and Developmental Evolution 304B 86CrossRefGoogle Scholar
Vargas, A. O.Fallon, J. F. 2005 The digits of the wing of birds are 1, 2, and 3. a reviewJournal of Experimental Zoology–Molecular and Developmental Evolution 304B 206CrossRefGoogle Scholar
Vickaryous, M.Olson, W. 2007 Sesamoids and ossicles in the appendicular skeletonFins Into Limbs: Evolution, Development, and TransformationHall, B.Chicago, ILUniversity of Chicago Press323Google Scholar
Waddington, C. H. 1953 Genetic assimilation of an acquired characterEvolution 7 118CrossRefGoogle Scholar
Wagner, G. P. 2007 The current state and the future of developmental evolutionFrom Embryology to Evo-Devo: A History of Developmental EvolutionLaubichler, M. D.Maienschein, J.Cambridge, MAMIT Press525Google Scholar
Wagner, G. P.Chiu, C. H. 2001 The tetrapod limb: a hypothesis on its originJournal of Experimental Zoology–Molecular and Developmental Evolution 291 226CrossRefGoogle ScholarPubMed
Wagner, G. P.Gauthier, J. A. 1999 1, 2, 3= 2, 3, 4: a solution to the problem of the homology of the digits in the avian handProceedings of the National Academy of Sciences of the United States of America 96 5111CrossRefGoogle ScholarPubMed
Wagner, G. P.Vargas, A. O. 2008 On the nature of thumbsGenome Biology 9CrossRefGoogle ScholarPubMed
Wang, B.Fallon, J. F.Beachy, P. A. 2000 Hedgehog-regulated processing of Gli3 produces and anterior/posterior repressor gradient in the developing vertebrate limbCell 100 423CrossRefGoogle ScholarPubMed
Wang, Z.Yuan, L. H.Rossiter, S. J. 2009 Adaptive evolution of 5'HoxD genes in the origin and diversification of the cetacean flipperMolecular Biology and Evolution 26 613CrossRefGoogle ScholarPubMed
Weatherbee, S. D.Behringer, R. R.RasweilerIV, J. J.Niswander, L. A. 2006 Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversificationProceedings of the National Academy of Sciences of the United States of America 103CrossRefGoogle ScholarPubMed
Weisbecker, V.Nilsson, M. 2008 Integration, heterochrony, and adaptation in pedal digits of syndactylous marsupialsBMC Evolutionary Biology 8CrossRefGoogle ScholarPubMed
Weissengruber, G. E.Egger, G. F.Hutchinson, J. R. 2006 The structure of the cushions in the feet of African elephants ()Journal of Anatomy 209 781CrossRefGoogle Scholar
Welten, M. C. M.Verbeek, F. J.Meijer, A. H.Richardson, M. K. 2005 Gene expression and digit homology in the chicken embryo wingEvolution and Development 7 18CrossRefGoogle ScholarPubMed
Werneburg, I. 2009 A standard system to study vertebrate embryosPloS One 4CrossRefGoogle ScholarPubMed
Westoll, T. S. 1943 The origin of the primitive tetrapod limbProceedings of the Royal Society of London B–Biological Sciences 131 373CrossRefGoogle Scholar
Whidden, H. P. 2000 Comparative myology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla)American Museum Novitates 3294 12.0.CO;2>CrossRefGoogle Scholar
Whitworth, D. J.Licht, P.Racey, P. A.Glickman, S. E. 1999 Testis-like steroidogenesis in the ovotestis of the European mole, Biology of Reproduction 60 413CrossRefGoogle Scholar
Woltering, J. M.Duboule, D. 2010 The origin of digits: expression patterns versus regulatory mechanismsDevelopmental Cell 18 526CrossRefGoogle ScholarPubMed
Wu, X. C.Li, Z.Zhou, B.-C.Dong, Z.-M 2003 A polydactylous amniote from the Triassic periodNature 426CrossRefGoogle ScholarPubMed
Xu, X.Clark, J. M.Mo, J. 2009 A Jurassic ceratosaur from China helps clarify avian digital homologiesNature 459 940CrossRefGoogle ScholarPubMed
Yalden, D. W. 1966 The anatomy of mole locomotionJournal of Zoology 149 55CrossRefGoogle Scholar
Young, R. L.Wagner, G. P. 2011 Why ontogenetic homology criteria can be misleading: lessons from digit identity transformationsJournal of Experimental Zoology–Molecular Development and Evolution 314B 165CrossRefGoogle Scholar
Young, R. L.Caputo, V.Giovannotti, M. 2009 Evolution of digit identity in the three-toed Italian skink : a new case of digit identity frame shiftEvolution and Development 11 647CrossRefGoogle ScholarPubMed
Zhang, G.Miyamoto, M. M.Cohn, M. J. 2006 Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeletonProceedings of the National Academy of Sciences of the United States of America 103 3180CrossRefGoogle ScholarPubMed
Zuzarte-Luís, V.Hurlé, J. M. 2002 Programmed cell death in the developing limbInternational Journal of Developmental Biology 46 871Google ScholarPubMed
Zuzarte-Luís, V.Hurlé, J. M. 2007 Apoptosis in fin and limb developmentFins Into Limbs: Evolution, Development, and TransformationHall, B.Chicago, ILUniversity of Chicago Press103Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×