EVOLUTION & DEVELOPMENT

3:1, 41–46 (2001)

©

BLACKWELL SCIENCE, INC.

41

Étienne Geoffroy St.-Hilaire: father of “evo-devo”?

Alec L. Panchen

Department of Marine Sciences, University of Newcastle-upon-Tyne, Newcastle-upon-Tyne NE1 7RU, UK; and Ecology Centre, University of Sunderland, Sunderland SR1 3SD, UK

Current address: 2 Dene Head, Ryton, Tyne and Wear, NE40 3QL, UK

SUMMARY

In the early decades of the nineteenth century,the most important disagreement among comparative anato-mists was not evolution versus “special creation” but betweenadvocates of “transcendental morphology” and those of tele-ological anatomy—form versus function. In France this di-chotomy was represented by the 1830–1832 public debatebetween Geoffroy St.-Hilaire (form) and Cuvier (function). Geof-froy’s aim was to establish links of homology (known to him

as “analogies”) between the four “embranchements” intowhich Cuvier had divided the animal kingdom. Despite thefanciful nature of some of his homologies, Geoffroy, who wasguided by his “

principe de connections

,” set in motion aschool of morphology, some of whose conclusions, notablythe homology of the dorsal surface of segmented inverte-brates with the ventral surface of vertebrates, has been cor-roborated by recent studies in developmental genetics.

INTRODUCTION

Elizabeth Gaskell’s last novel,

Wives and Daughters

, was setrather vaguely in the late 1820s or the 1830s and was firstpublished in book form in 1866, the year after her death. Hernaturalist hero Roger Hamley comes to the attention of thescience world as the author of a paper defending the views ofGeoffroy against those of Georges Cuvier. He is even invitedby a local aristocratic naturalist to meet “M. Geoffroi St. H.”[

sic

] and subsequently goes to Africa on a subsidized collect-ing expedition. The heroine of

Wives and Daughters

, MollyGibson, surprises the same aristocratic naturalist by herknowledge of Cuvier’s

Le Règne Animal.

For in the early nineteenth century, the great divisionamong systematic biologists was not between evolutionistsand special creationists, although Lamarck had first pro-posed his theory of evolution in lectures in 1800 (Lamarck1802) and produced his principal statement in 1809. Rather,it was between the advocates of teleology—the expla-nation of anatomical features in terms of adaptation, not-ably Cuvier (1769–1832)—and those of “transcendentalmorphology,” the search for homologies rather than adap-tive explanations, notably Geoffroy St.-Hilaire (1772–1844).These two, both professors at the Muséum d’Histoire Na-turelle in Paris, had been close friends and colleagues. Butduring the 1820s their theoretical views, reinforced by pro-fessional rivalry, had diverged until in 1830 their differ-ences burst forth in a famous public row that continued untilCuvier’s death in 1832. The row with its background andaftermath are chronicled by Appel (1987; see also Russell1916).

CUVIER

Cuvier was utterly opposed to the philosophical idealismrepresented by the research program of transcendental mor-phology, and particularly to Geoffroy’s claim that there wasa common morphological plan to the whole animal kingdom.Cuvier’s final stance was that of a pure teleologist—namely,that all structures must be explained in terms of function. Hisown classification, which was based on functional princi-ples, was to divide the animal kingdom into four

embranche-ments

with no common plan of homologies between them.This classification was a

de facto

rejection of an ancient con-cept—that of the great ladder of life, the

scala naturae

(Lovejoy 1936), which dominated the view of most natural-ists in the early nineteenth century as it had done with philos-ophers and naturalists in the eighteenth century.

Cuvier’s

embranchements

were proposed on a basis abso-lutely at odds with the idea of the

scala.

Classification wasto be based as nearly as possible on two interrelated princi-ples, the “conditions of existence” (adaptation) and the “cor-relation of parts.” He explained the first thus:

Since nothing can exist that does not fulfil the conditions whichrender its existence possible, the different parts of each being mustbe coordinated in such a way as to render possible the existence ofthe being as a whole, not only in itself, but also in its relations withother beings, and the analysis of these conditions often leads togeneral laws which are as certain as those which are derived fromcalculation or from experiment.

[Cuvier 1817, i., p.6 – translation from Russell 1916 (1982) p. 34]

While there is reference to “other beings,” Cuvier’s con-ditions were not comparable to an ecological view that the

42 EVOLUTION & DEVELOPMENT

Vol. 3, No. 1, January–February 2001

phrase might invoke today—the other beings were involvedin direct interaction, such as in a predator-prey relationship,rather than in a niche in the environment. Cuvier was a com-parative anatomist, not a naturalist.

The principle of correlation arises directly from the condi-tions of existence and leads to Cuvier’s claim that, given onepart of an animal, one can predict the nature of some unrelatedpart of its anatomy, a claim both reinforced by, and used in, hiswork as the pioneer vertebrate palaeontologist: “In a word, theform of the tooth implies the form of the condyle; that of theshoulder blade that of the claws, just as the equation of a curveimplies all its properties” [quoted in Russell 1916 (1982), p. 36]

At first Cuvier (1800–1805) simply divided the animal king-dom into nine classes, but in the

Règne Animal

(1817), he de-veloped the principle of the subordination of parts. He decidedthat major taxa should be defined by the functionally most im-portant characteristics. This led to the delineation of the four

embranchements

based primarily on the animal (as opposed toplant) feature of a neuromuscular system: (1) Vertebrates havea single dorsal nerve cord and brain and an axial skeleton; (2)Molluscs have muscles attached to the skin and shell and a ner-vous system of separate ganglia; (3) Articulates (largely arthro-pods and annelids) have an external skeleton and paired ven-tral nerve cords (but lack “proper” blood vessels); (4) Radiates(echinoderms, cnidarians, and “waste-basket” groups) have ill-defined or no nervous systems, and are radially symmetrical butshow sensitivity. There was no principle that dictated any sortof relationship between the

embranchements.

GEOFFROY

The discovery of such a relationship between Cuvier’s

em-branchements

was one of the principal aims of Geoffroy’s ca-reer. He was guided by two concepts: (1) the recognition ofhomology (referred to by him as “

analogie

” in contrast to pres-ent usage) by the “

principe de connections

,” and (2) the “

loi debalancement

,” the law of compensation. We can illustrate theprinciple of connections by reference to Geoffroy St.-Hilaire’s(1818) attempt to find, in the skull of mammals, the homo-logues of the apparent extra bones in the skull of bony fish. Forit was claimed by Geoffroy that, in his system, every structurein one animal must have its homologue in another. So havingestablished, as he thought, that the tympanic cavity of mam-mals was the homologue of the gill chamber of fishes, he usedthe principle of connections to equate (wrongly) the middle earossicles of mammals with the opercular bones of fishes, thus:

Mammals Fish

Stapes OperculumMalleus InteroperculumLenticular and Incus SubopoerculumTympanic Preoperculum

He stated the principle of connections as follows. “Na-ture, I have said above, tends to cause the same organs to re-appear in the same number and in the same relations, and itvaries to an infinite degree only in their form. According tothis principle, in the determination of the bones of the headof fishes, I will never have to decide according to consider-ation of their form, but only according to their connections”(Geoffroy St.-Hilaire 1807, quoted by Appel 1987, p. 89).Homology between structures in two animals is to be judgednot by anatomical similarity, but by the connection of thosestructures to the same anatomical features.

The difference between anatomical features of homolo-gous structures is then explained by the law of compensa-tion. This law states that if any anatomical feature is rela-tively overdeveloped within a particular animal species,some other feature will be relatively underdeveloped. An im-portant point is implicit in the law. In agreement with Cuvier,Geoffroy rejected the

a priori

assumption of the

scalanaturae

(although he did allow this belief to lapse some ofthe time). In order to elucidate the homology of a particularstructure in a range of animal taxa, one looked for the animalin which that structure was most completely developed. Thestandard of comparison was not the animal highest (or low-

Fig. 1. Geoffroy in the 1820s. [from Appel (1987), with permission]

Panchen

Geoffroy: father of “evo-devo”?

43

est) on the

scala

or at the top (or bottom) of the evolutionarytree. An example is Geoffroy’s work on the homology of thevertebrate sternum. According to Geoffroy St.-Hilaire (1818),the vertebrate sternum was most completely developed in theplastron of the tortoise in which he identified nine bones(Fig. 2). The sternum in all other vertebrates must then be in-terpreted in terms of these nine bones—there must be homol-ogy within the overall structure as well as the use of the cri-terion of connections to elucidate its overall homology inrelation to other structures. The law of compensation thendictated that if one of the bones of the sternum was exces-sively developed, as in the sternum of birds, the others wouldbe correspondingly reduced. Overall, the law asserted that

there was a limited amount of material from which an indi-vidual animal could be developed. If, in its development, thewhole sternum was excessively represented, other structureswould be reduced in compensation.

It is worth noting that both the principle of connectionsand the law of compensation make it clear that Geoffroy wasaiming at rules to establish transformational rather than taxichomologies in Patterson’s (1982) terminology. The ruleswere established for the recognition of homologous struc-tures of sometimes very different appearance, rather than therecognition of taxonomic features. The transformations im-plicit in transformational homology need not, of course, beevolutionary ones. Richard Owen sought transformations

Fig. 2. The Loi de Balancement: homologies in the vertebrate sternum. [from Geoffroy St.-Hilaire (1818). N.B. No. 21—the plastron ofa tortoise with its nine ossifications]

44 EVOLUTION & DEVELOPMENT

Vol. 3, No. 1, January–February 2001

from his vertebrate archetype (Panchen 1994), without anyphylogenetic implication. Geoffroy’s aim was to demon-strate the unity of plan of the animal kingdom, but apparentlynot to establish a taxonomic or phylogenetic hierarchy.

HOMOLOGUES BETWEEN

EMBRANCHEMENTS

?

At first Geoffroy confined his study of homologues withinwhat were to be Cuvier’s

embranchements

, particularlywithin vertebrates and later within articulates (between in-sects and crustaceans). But even as early as 1795, when hewas only 23, he had enunciated his guiding principle in anaddendum to a memoir on lemurs:

It seems that nature has enclosed herself within certain limits andhas formed all living beings on only one unique plan, essentially thesame in its principles, but which she has varied in a thousand waysin all its accessory parts . . . The forms in each class of animals, how-ever varied, all result in the end from organs common to all. Naturerefuses to employ new ones. Thus all the most essential differenceswhich affect each family within the same class come only from an-other arrangement, from another complication, in short from a mod-ification of these same organs. [Geoffroy St.-Hilaire 1796: quotedby Appel 1987, p. 28]

His first attempts to cross the Cuvierian boundary werepublished in 1820 in a memoir, in which he united the Ver-tebrata of Cuvier (“

Hauts-Vertébrés

”) with the Articulata(“

Dermo-Vertébrés

”). This act incorporated two of Geof-froy’s most famous hypotheses: first, the segmental ring ofan arthropod exoskeleton is the homologue of a vertebra of avertebrate, with the arthropod appendages corresponding tovertebral ribs (“every animal lives within or without its ver-tebral column”); and second, the anatomy of any articulate(“

dermo-vertébré

”) corresponds to that of a vertebrate ro-tated through 180

8

about its long axis. The articulate nervecord(s) is ventral, whereas that of a vertebrate is dorsal.

The first theory, the homology of dermal segment andvertebra, sounds like pure fantasy. Geoffroy’s explanationwas that insects have a poorly developed blood system, sothat all their bodily development was promoted by the ner-vous system. However, the second theory is more plausiblebecause of developments in “evo-devo” biology. The ideawas revived by Arendt and Nübler-Jung (1994), and withinthe last few years it has been demonstrated that there is acommon plan of intercellular signalling, resulting in oppo-site orientation of the body in vertebrates (

Xenopus

) and in-sects (

Drosophila

) (De Robertis and Sasai 1996; Oelge-schläger et al. 2000). All three sets of authors credit GeoffroySt.-Hilaire (1822) as the proposer of the theory that the ven-tral side of arthropods is homologous to the dorsal side ofvertebrates. Naturally, however, they give an evolutionaryinterpretation to the homology—rotation one way or theother must have occurred in phylogeny.

GEOFFROY AND EVOLUTION

Geoffroy was in fact an evolutionist late in his career, nodoubt influenced by his elderly colleague Lamarck (1744–1829), but in general this seemed to have little effect on hisaim to establish a pure science of morphology. There is,however, one important conclusion that Geoffroy did reachas a result of his evolutionary belief.

He was first moved to accept that evolution had occurredby his study of the fossil skulls of two closely related speciesof crocodilian,

Steneosaurus

and

Teleosaurus

, from theFrench Jurassic (Geoffroy St.-Hilaire 1833). Superficially,these species strongly resembled the extant gavials—Indianlong-snouted crocodilians. Surely, Geoffroy argued, it is moreprobable that there is an ancestor-descendant relationshipthan that there had been a series of extinctions followed byspecial creation of crocodilians, as Cuvier’s theory of catas-trophism seemed to demand.

Geoffroy even proposed a mechanism, different from thatof Lamarck (and not of course natural selection!). Over geo-logical time, there had been a decrease in the “energy” of at-mospheric oxygen that affected the growth and arrangementof the arteries of the developing fetus, thus producing adap-tive change. This theory of mechanism was inspired by thework of Geoffroy and his faithful protegé, Etienne Serres, on“teratology” and illustrates Geoffroy’s lapse into acceptanceof the

scala naturae.

Teratology is the study of deformed andaborted fetuses and led to Serres’ theory of “arrests of devel-opment,” one of the first coherent statements of the conceptof recapitulation: that the human fetus in its development tothe adult form parallels the order of the

scala naturae

towardthe terminal human condition. This concept of recapitulationwas characterized by Russell (1916) as the “Meckel-SerresLaw.” Serres was not an evolutionist, but after the generalacceptance of evolution, the concept of recapitulation wasreinterpreted as a parallel between phylogeny and individualdevelopment, notably by Haeckel (1866).

The general acceptance of phylogeny, however, made lit-tle difference to the methods used by morphologists. Theiraim in the latter part of the nineteenth century was still theelucidation of homologies guided by Geoffroy’s principle ofconnections. They interpreted their results in terms of the re-construction of phylogeny. Thus, in comparing the dorsal as-pect of an invertebrate with the ventral aspect of a vertebrate,morphologists saw themselves not simply as seeking homo-logues between the two, but also as studying “the origin ofvertebrates.”

More positively, embryology and larval developmentwere incorporated into morphological studies. In 1866, Al-exander Kowalevsky proposed for the first time the origin ofvertebrates from an ascidian larva, and a rival camp revivedthe dorsoventral theory of Geoffroy. Leydig (1864) had citedhistological similarity between the nerve cords of insects and

Panchen

Geoffroy: father of “evo-devo”?

45

vertebrates. Then, Carl Semper (1876) suggested that arthro-pods and vertebrates had diverged from annelids, and thatthe proper study should be of the latter as the ancestral group(Fig. 3). Semper’s paper concludes with a stirring defence ofGeoffroy’s proposal that vertebrates and Cuvier’s “articu-lates” together form a natural group.

Perhaps the best-known advocate of the “reverse annelid”theory was Anton Dohrn, founder of the Zoological Stationat Naples. In his book

Der Ursprung der Wirbelthiere

, Dohrn(1875) claimed, in the spirit of Geoffroy, that no new struc-ture need be proposed in mapping from an annelid to a ver-tebrate; but both he and Semper had the same problem in theorigin of the vertebrate mouth, which was ventral in articu-lates but also ventral in vertebrates. Semper opted for an ob-scure pit seen in leeches as the homologue of the vertebratemouth. Dohrn proposed that the mouth was a neomorph, de-spite his own claim, pointing out that the vertebrate mouthappeared late in ontogeny.

The study of morphology, still guided by the

principe deconnections

, persisted into the twentieth century, and aspectsof its history are chronicled by Bowler (1996). But increas-ingly it was held in low esteem so that in the development ofthe “synthetic theory” of evolution in the 1930s and ’40s,comparative anatomy (and comparative embryology) weregiven little weight. The picture has of course changed radi-cally in recent years with the flowering of developmental ge-netics and “evo-devo.”

TWO QUESTIONS

Hence the questions implicit and explicit in the title of thisarticle remain: the former is to ask whether the designationof long-dead luminaries as “fathers” (or “mothers”) of cur-rent science is a worthwhile exercise; the latter, if the answerto the first is “yes,” why in this particular case should onesettle on Geoffroy?

By “father” of a current scientific discipline, I mean theperson who first took a scientific stance that initiated the de-velopment of that discipline. Other eminent workers, such asthose discussed in the previous section, obviously followed.But to quote Gould (1977, p. 1): “The essential questions of

a discipline are usually specified by the first competentthinkers to enter it. The intense professional activity of latercenturies can often be identified as so many variations on aset of themes. The arrow of history specifies a sequence ofchanging contents within which the same old questions areendlessly debated . . .”

In the case of comparative anatomy, the two rival ap-proaches to the interpretation of animal forms were high-lighted by the Cuvier–Geoffroy debate and represent, inGould’s phrase, “the essential questions of [the] discipline.”Should one interpret the findings of comparative anatomyprincipally in terms of adaptation, or in terms of relationship(whether attributed to evolution or some other explanatoryprinciple)? Since the general acceptance of evolution, rela-tionship has been attributed to phylogeny, but the essentialquestion persists and is argued over today. Perhaps those whoargue about the rival claims of adaptation (usually attributedto natural selection) and homology (now attributed to phylog-eny) as the primary approach to the study of comparativeanatomy should be aware that they are staging a re-run of theCuvier–Geoffroy confrontation: Cuvier as father of pan-adaptationism, Geoffroy as father of animal monophyly?

But, again, why Geoffroy? He was not the first to employthe concept of homology—that goes back at least to Aristotle(Panchen 1994, 1999). Nor can one imagine that some of hismore fanciful hypotheses would get past the modern proto-col of peer review. He occasionally fantasized wildly, evenby the standards of his own time. Perhaps the most egregiousexample is the assertion that drove him and Cuvier into theirpublic debate (Appel 1987). Two young and obscure natural-ists, Pierre-Stanislas Meyranx and Laurencet (who is so ob-scure that even his given name is not recorded) submitted apaper on the organization of molluscs. It was never pub-lished, but Geoffroy picked up with glee their incidental con-clusion that a cuttlefish (a cephalopod mollusc) had the samearrangement of organs as a vertebrate bent backwards at theumbilicus, so that the nape of the neck was attached to thebuttocks—again two of Cuvier’s

embranchements

united!Cuvier, however, was easily able to refute the proposal.

And yet another apparently wild proposal by Geoffroy,the invertebrate/vertebrate dorso-ventral theory, has beencorroborated by recent studies in “evo-devo.” The theorywas not corroborated by conventional comparative anatomy,but using techniques that have been developed over recentdecades and would have been incomprehensible to Geoffroy.But that could be said of Darwin vis-à-vis the “SyntheticTheory” of evolution of the 1930s and ‘40s, with its compo-nent of population genetics. The development of evolutionand development as a discipline has shown that there are ho-mologies to be found between phyla at the level of develop-mental genetics that vindicate Geoffroy’s expansive vision.

Arthur (1997) has suggested that there is a difference be-tween the morphological homologies to which Geoffroy as-

Fig. 3. An early twentieth-century view of the annelid-vertebratetheory. [figure and original legend from Wilder (1909)]

46 EVOLUTION & DEVELOPMENT

Vol. 3, No. 1, January–February 2001

pired and the type of homology represented by the dorsoven-tral signalling system. Arthur describes the latter as causal,explaining the morphological outcome. This applies also tothe example that he cites—one that is at an even higher level,proposed as a diagnostic feature of all animals, an autapo-morphy of the Kingdom Animalia. The phylotypic stage ofan animal embryo was defined as that stage at which all thepotential body parts are in their definitive positions relativeto one another, but as yet undifferentiated cells (Sander1983). Slack et al. (1993) suggest that during the phylotypicstage (better thought of as the “phylotypic period;” Richard-son 1999) in any animal there exists and is active a group ofgenes (the Hox cluster and others) that are responsible forpositional information. These genes and the system they em-body are homologous throughout the animal kingdom—truly the sort of pan-

embranchement

homology to whichGeoffroy aspired and proposed in the same spirit.

Geoffroy’s ambition was “to found a science of pure mor-phology” (Russell 1916, 1982). According to Russell, “hefailed: his failure showed once and for all, that a pure mor-phology of organic forms is impracticable.” Russell mayhave been right at the level of comparative anatomy, but withthe current techniques of “evo-devo,” we now know that hewas wrong.

Acknowledgments

The substance of these musings was originally presented as an in-troductory lecture at a meeting on Evolution and Development heldin Sunderland on 12 September 2000, and organized by WallaceArthur and Mike Coates. I was grateful for the invitation to speak.I am also indebted to both organizers as well as two reviewers fortheir comments on the manuscript of this paper. Several versions,including the final one, were typed at Sunderland by Carolyn Stout.

REFERENCES

Appel, T. A. 1987.

The Cuvier-Geoffroy Debate: French Biology in the De-cades before Darwin.

Oxford University Press, New York.Arendt, D., and Nübler-Jung, K. 1994. Inversion of the dorsoventral axis.

Nature

371: 26.Arthur, W. 1997.

The Origin of Animal Body Plans: A Study in Evolution-ary Developmental Biology.

Cambridge University Press, Cambridge.Bowler, P. J. 1996.

Life’s Splendid Drama: Evolutionary Biology and theReconstruction of Life’s Ancestry 1860–1940.

University of ChicagoPress, Chicago.

Cuvier, G. 1800–1805.

Leçons d’Anatomie Comparée de Georges Cuvier,Recueillis et Publiées sous ses Yeux par C. Dumeril.

[vol. 1–2: 1800, vol.3–5: 1805] Bandouin, Paris.

Cuvier, G. 1817.

Le Règne Animal Distribué d’après son Organisation PourServir de Base à l’Histoire Naturelle des Animaux . . .

[4 vols]. Deterville,Paris.

De Robertis, E. M., and Sasai, Y. 1996. A common plan for dorsoventralpatterning in Bilateria.

Nature

380: 37–40.

Dohrn, A. 1875.

Der Ursprung der Wirbelthiere und das Princip des Func-tionswechsels: Genealogische Skizzen.

Wilhelm Englemann, Leipzig.Gaskell, E. C. 1866.

Wives and Daughters. An Every-day Story.

Smith, El-der & Co., London.

Geoffroy St.-Hilaire, E. 1796. Mémoire sur les rapports naturels des MakisLemur, L., et description d’une espèce nouvelle de mammifère.

Maga-

sin encyclopédique

[2

e

année] 1: 20–50.Geoffroy St.-Hilaire, E. 1807. Considérations sur les pièces de la tête os-

seuse des animaux vertébrés, et particulièrement sur celles du crâne desoiseaux.

Ann. Mus. Hist. Nat.

10: 342–365.Geoffroy St.-Hilaire, E. 1818.

Philosophie Anatomique, vol. I. Des OrganesRespiratoires sous le Rapport de la Determination et de l’Identité de leursPièces Osseuses.

J. B. Baillière, Paris.Geoffroy St.-Hilaire, E. 1820. Sur une colonne vertébrale et ses côtes dans

les insectes apiropodes.

Ann. générales des Sci. Physiques

5: 96–132.Geoffroy St.-Hilaire, E. 1822. Considérations générales sur la vertébre.

Mem. Mus. d’Hist. Nat.

9: 89–119.Geoffroy St.-Hilaire, E. 1833. Divers mémoires sur de grands sauriens

trouvés à l’état fossile vers les confins maratimes de la basse Nor-mandie, attribués d’abord au crocodile . . .

Mém. de l’Acad. Sci.

12: 63–92.

Gould, S. J. 1977. Eternal metaphors of palaeontology. In A. Hallam (ed.)

Patterns of Evolution.

Elsevier Scientific, Amsterdam, pp. 1–26.Haeckel, E. 1866.

Generelle Morphologie der Organismen

(2 vols.). Walterde Gruyter, Berlin.

Kowalevsky, A. 1866. Entwickelungsgeschichte der einfachen Ascidien.

Mem. de l’Acad. Sc. St Petersbourg.

7

th

Ser., 10, No. 15:1–19.Lamarck, J.-B. P. A. de M. 1802.

Recherches sur l’Organisation de CorpsVivant, et Particulierement sur son Origine . . .

Maillard, Paris.Lamarck, J.-B. P. A. de M. 1809.

Philosophie Zoologique, ou Exposition

des Considerations Relatives à l’Histoire Naturelle des Animaux . . .

[2 vols.] Dentu, Paris.Leydig, F. von 1864.

Vom Bau der Thierischen Körpers. Handbuch der Ver-gleichenden Anatomie.

H, Laupp’schen buchhandlung, Tubingen.Lovejoy, A. O. 1936.

The Great Chain of Being.

Harvard University Press,Cambridge, MA.

Oelgeschläger, M., Larrain, J., Geissert, D., and De Robertis, E. M. 2000.The evolutionarily conserved BMP-binding protein twisted gastrulationpromotes BMP signalling.

Nature

405: 757–763.Panchen, A. L. 1994. Richard Owen and the concept of homology. In B.K.

Hall (ed.).

Homology: The Hierarchical Basis of Comparative Biology

.Academic Press, San Diego, pp. 21–62.

Panchen, A. L. 1999. Homology—history of a concept. In B.K. Hall (chair).

Homology (Novartis Foundation Symposium

222). Wiley, Chichester,pp. 5–18.

Patterson, C. 1982. Morphological characters and homology. In K. A. Joy-sey and A. E. Friday (eds.).

Problems of Phylogenetic Reconstruction

.Academic Press, London, pp. 21–74.

Richardson, M. K. 1999. Vertebrate evolution: the developmental originsof adult variation.

BioEssays

21: 604–613.Russell, E. S. 1916.

Form and Function: A Contribution to the History ofAnimal Morphology.

John Murray, London. (Russell, E. S. 1982. re-printed with a new introduction by George V. Lauder. Chicago Univer-sity Press, Chicago.)

Sander, K. 1983. The evolution of patterning mechanisms: gleaning from in-sect embryogenesis and spermatogenesis. In B. C. Goodwin, H. Holder,and C.C. Wyllie (eds.).

Development and Evolution.

Cambridge Uni-versity Press, Cambridge, pp. 137–159.

Semper, C. 1876. Die Verwandtschaftsbeziehungen der gegliedertenThiere.

Arbeiten aus dem Zool.-zootom. Inst. Würzburg

3: 9–404.Slack, J. M. W., Holland, P. W. H., and Graham, C. F. 1993. The zootype

and the phylotypic stage.

Nature

361: 490–492.Wilder, H. H. 1909.

History of the Human Body.

Henry Holt, New York.