© 2000 by The Society for Integrative and Comparative Biology
Balfour, Garstang and de Beer: The First Century of Evolutionary Embryology1
1 Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1
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Evolution has been integrated with embryology during two great periods: the latter half of the 19th C as evolutionary morphology/embryology, and the latter third of the 20th C as evolutionary developmental biology. My mandate was to use the contributions of three embryologists/morphologists: Francis (Frank) Balfour (1851–1882), Walter Garstang (1868–1949) and Gavin de Beer (1899–1972) to discuss the foundations of evolutionary embryology in the UK from 1870 (when "every aspiring zoologist was an embryologist, and the one topic of professional conversation was evolution," Bateson, 1922
, p. 56), through the 1920s ("ontogeny does not recapitulate phylogeny, it creates it," Garstang, 1922, p. 81) to the 1970s ("homology of phenotypes does not imply similarity in genotypes," de Beer, 1971, p. 15). Evolutionary embryology was driven by a comparative embryological approach that sought homology of adult structures in germ layers and ancestry in embryos, and sought to differentiate larval adaptations from retained ancestral characters. An initial emphasis on a phylogenetic mechanism (recapitulation) slowly gave way to more mechanistic approaches that included heterochrony and the integration of embryology with physiological genetics. Germ layers, homology, larval evolution, larval origins of the vertebrates, paedomorphosis and heterochrony underpinned the origins of evolutionary embryology, and so I discuss each of these topics. |
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The foundation of evolutionary morphology/embryology built in the late 19th C rested on: a knowledge of shared and conserved developmental stages; the universality of germ layers (the cell layers from which all tissues and organs form) as the fundamental units from which the embryos of all multicellular animals are constructed; an embryological criterion of homology rooted in germ layers; and linkage of embryology to classification through the organization of the animal kingdom into diplo- and triploblastic grades. During the 19th century, the generality and importance of germ layers became increasingly appreciated. They were first recognized in chicken embryos by Pander in 1817. Rathke (1825)
identified equivalent germ layers in a decapod crustacean, von Baer (1828) discovered germ layers in the embryos of other vertebrates, Huxley (1849) showed that the outer and inner layers of vertebrate embryos3 were homologous with the two germ layers seen in adult coelenterates, extending the germ layer concept from embryos to adults and from embryology to evolution, while Lankester (1877) gave germ-layer theory an even more substantial role when he divided the animal kingdom into three grades—Homo-, Diplo- and Triploblastica.
Theories of relationships and ancestry, which had previously rested on evidence from adults, now relied on embryological evidence. Embryology provided the criteria for homology and so was the subject to study if relationships and ancestry were to be uncovered. Thus, for several decades after Darwin published The Origin of Species, germ-layer theory, evolutionary morphology/embryology, the use of embryological criteria for homology, and embryological archetypes dominated zoology (see Hall, 1998a, b, 1999a, 2000). My task at the conference was to evaluate the contributions made to the first century of evolutionary embryology by three individuals—Francis Balfour, Walter Garstang and Gavin de Beer. My remit and the space available allow neither a comprehensive analysis of their work nor a more extensive analysis of evolutionary embryology.
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Francis (Frank) Maitland Balfour (1851–1882) took up evolutionary embryology while he was a Cambridge undergraduate. Michael Foster, who arrived at Trinity College as Praelector in Physiology at the same time (1872), gave Balfour the task of determining whether Hensen's node and the primitive streak of the embryonic chick bore any structural or functional relationship to the blastopore of amphibian embryos. Foster realized that any relationship would illuminate homology and therefore vertebrate origins and relationships. Balfour (1873a, b)
demonstrated the homology, setting the stage for a brief but enormously influential career, a career that elucidated the importance of evolutionary embryology as the way to understand vertebrate and invertebrate origins. The culmination of his career was the two-volume Treatise on Comparative Embryology (1880–1881), which was infused with evolutionary thinking. In 1882, Cambridge created a Professorship in Animal Morphology for the 32-yr-old Balfour. His death just seven weeks later in an alpine climbing accident robbed evolutionary embryology of its most promising advocate. Balfour's approach was based firmly on homology of the germ layers and the ability of embryological homology to reveal phylogenetic relationships. The prevailing dogma asserted that structures in different organisms could only be compared if they were homologous, that homologous structures arose from the same germ layer, and that embryos repeated (recapitulated) their evolutionary history. Embryology thus offered the way to uncover relationships and origins. Given the discovery in the mid-19th century of the chordate affinities of the hemichordates and ascidians, the nature of amphioxus, and vigorously contested rival theories for invertebrate ancestors of the vertebrates, a bright young undergraduate was inevitably drawn into evolutionary embryology. Writing about the 1870s, William Bateson, who for a time was involved in such studies, said:
Morphology was studied because it was the material believed to be the most favorable for the elucidation of the problems of evolution, and we all thought that in embryology the quintessence of morphological truth was most palpably presented. Therefore every aspiring zoologist was an embryologist, and the one topic of professional conversation was evolution (Bateson, 1922, p. 56).4
Germ layers, homology and mechanisms of development
Balfour (1873a–c) used surface views (what we now call whole mounts) and histological sections (which he cut by hand) of chick embryos up to about 40 hr of incubation to report development of the blastoderm, primitive groove and blood vessels. (Paradoxically, the development of instruments [microtomes] for section-cutting enabled great advances to be made in microscopic anatomy and embryology but made embryology one of the most "technological" and therefore inaccessible subjects in natural history.)
Using Lankester's terms epiblast, hypoblast and mesoblast for the embryonic germ layers,5 Balfour described chick ectoderm and endoderm for the first time in English. He emphasized that the endoderm arises from preexisting cells (the transformation "of a cell of one kind into a cell of a totally different character" [1873a, p. 269]) and confirmed the origin of the mesoderm from large formative cells that move between ecto- and endoderm and demonstrated (in these and subsequent studies with dogfish; see below) that mesoderm arises independently from either ectoderm or endoderm. He also emphasized that differences in mode of formation rather than initial differences in appearance distinguish mesoderm from endoderm (i.e., that developmental relationships reveal homology), and placed his conclusion into two phylogenetic contexts:
- endoderm and mesoderm in chick embryos do not show any evidence of the primary mode of formation (by which he meant the pattern of involution seen in amphibians); and
- mesoderm formation is secondary in invertebrates but primary in birds.
Although spurred into undertaking the work by Haeckel's (1866) theory of the relationship between ontogeny and phylogeny, here, in his very first paper, the 22-yr-old undergraduate distinguishes secondary embryonic adaptations from primary, ancestral patterns and avoids the excesses of Haeckel's interpretations. For example, Balfour's work contained no simple linear progression from invertebrates 
vertebrates humans, although such ideas were in abundance (see Hall, 1998a, b, 1999b). The recognition that not all embryonic features reveal ancestral patterns is central to the informed extrapolation from ontogeny to phylogeny developed by Balfour and Garstang (see below).
Having shown a familiarity with the phylogenetic importance of germ layers, in his third paper, on the developing blood system Balfour also demonstrated an awareness of an important relationship between germ layers, patterns of development and homology, arguing that "It is perhaps, doubtful whether a system of vessels arising in this way [by aggregation] can be considered homologous with any vascular system which takes its origin from channels hollowed out in between the cells of the mesoblast" (1873c, p. 281); structures could not be homologous if the mechanisms of their development were so very different.
Following these studies on chick embryology, Balfour went on to describe the embryology of the dogfish, research undertaken in 1872 as the first British scientist to occupy a table at Anton Dohrn's new Stazione Zoologica Napoli. Balfour had much to say about homology and formation of the "segmentation cavity" (the blastocoele), which "appears, however, to have somewhat different relations to the blastoderm than the homologous structure in other vertebrates" (1874, p. 332). As in chick development, Balfour identifies the three germ layers and makes specific and unexpected comments on the origin of the mesoderm. "But there is another and, in some ways, rather a tempting view [for the origin of the mesoblast], viz. to suppose that the epiblast, where it becomes continuous with the hypoblast, in reality becomes involuted, and that from this involuted epiblast are formed the whole mesoblast and hypoblast" (1874, p. 336).
Endoderm and mesoderm form from the lower layer of cells. Why then, asks Balfour, are hypoblast and epiblast continuous? His explanation grouped vertebrates on the basis of two broad classes of development. One group—including amphioxus, lampreys, sturgeons and amphibians—displays the primitive condition, with holoblastic eggs and involution of the endoderm through a blastopore. The second, which includes elasmobranchs, bony fishes, reptiles and birds, displays a secondary adaptation necessitated by the presence of excessive amounts of yolk. These animals have meroblastic eggs and infold the endoderm through a primitive streak. Mammals are missing from this list, an omission Balfour subsequently corrected by having several of his students investigate the early embryology of selected placental mammals, marsupials and monotremes: Walter Heape (the mole), Richard Assheton (rabbits), Joseph Lister (kangaroo) and William Caldwell (platypus).
Balfour saw a transition in the dogfish between these two great types of vertebrate development. The dogfish was a primitive type providing evidence of vertebrate ancestry. He identified continuity of ecto- and endoderm in the dogfish as a remnant of the primitive condition of involution through a circular blastopore. In discussing development beyond the germ-layer stage, Balfour focused on the origin of the notochord "as a thickening of the hypoblast," and saw the significance of an organ developing from a different layer from that which gave rise to it in an ancestor—mesoderm and notochord arising from the hypoblast in dogfish, but as an independent layer in birds—as the issue of whether homologous structures must share a common developmental origin. His evidence in favor of such a shift is instructive of his thinking and acceptance of Darwinian ideas:
I see no reason for doubting that the embryo in the earliest periods of development is as subject to the laws of natural selection as is the animal at any other period. Indeed, there appear to me grounds for the thinking that it is more so. (Balfour, 1874, p. 343)
Balfour published a further series of papers on dogfish embryology and gathered them together in 1878 into a Monograph on the Development of Elasmobranch Fishes. Lankester (who in 1873 had advocated embryology as the chief means of detecting homology) reviewed the monograph, drawing particular attention to Balfour's recognition of the homology of the blastopore with the blastodisc, and of the archenteron, notochord, head segments, paired and unpaired fins6 throughout the vertebrates. Balfour's identification of homologous structures throughout the vertebrates and homologous germ layers throughout the animal kingdom were seen as especially important additions to fundamental knowledge. The chief significance of the monograph, however, was in phylogenetic information revealed by the embryos of elasmobranch fishes:
...we have in these fishes the nearest living representatives of the common ancestors of the great group of Gnathostomous Craniate Vertebrata, and it was to be expected that a full knowledge of their ontogeny or individual development would carry us yet further back in the line of primitive vertebrata, and yield a mass of explanatory evidence, exhibiting the development of complex and heterogeneous structures from simpler and more homogeneous forms, likely to serve as a satisfactory starting point for all Vertebrate morphology. (Lankester, 1878, p. 113)
Balfour wrote his last substantive word on homology of the germ-layers in a paper (1880a)7 that was also included as a chapter in the Treatise. Now Balfour is unsure about the veracity of hypotheses concerning the mode of origin and homologies of the germ layers. "...there are few embryologists who would venture to assert that any hypotheses ...as to the mode of origin of the homologies of the germinal layers, have more than a tentative value" (1880a, pp. 247–248). Now he is "summarising the facts, and critically examining the different theories," rather than "dogmatically supporting any definite views of my own" (ibid, p. 248). Beginning with grand principles and significant questions—how did the Metazoa arise? how many lines of metazoan evolution are there? can homology of the germ layers be demonstrated?—the paper ends with a whimper. There is no grand pulling-together of his analyses, no summary of answers to the three great questions posed. Does this reflect Balfour's indecision over answers to the questions, a reluctance to come out against a strict recapitulationist interpretation of embryonic development and evolution or—despite his claim to the contrary—a dogmatic adherence to his views, especially on the origin of the mesoderm? Why is the origin of mesoderm from hypoblast in some groups not regarded as a secondary adaptation? After all, Balfour argued very strongly for natural selection acting throughout life history, including early in embryology. I believe the answer lies in the supremacy of the germ-layer theory. So entrenched was a belief in the constancy of germ layers that Balfour extended that constancy to an inability of the primary germ layers to change or adapt through evolution. He did, however, allow for a "general homology" between the primary germ layers, but without indicating any distinction between "complete" and "general" homology.
Balfour's morphology laboratory at Cambridge attracted such students as William Bateson, D'Arcy Thompson, Henry Fairfield Osborn, Adam Sedgwick and Walter Heape. Most became disenchanted with evolutionary embryology. Bateson and Weldon moved into genetics, Osborn and Scott into palaeontology. Although he began by pursuing germ layers, Adam Sedgwick, Balfour's successor at Trinity College, did a complete about-face, rejecting germ-layer and cell-theories entirely: to him the cell theory was a phantom. When extended to the germ layers it was the "layer phantom" (1894, p. 95). Caldwell (who had discovered the mode of reproduction in the platypus), left Science altogether, moving into paper manufacture.
Larvae, larval adaptations and natural selection
[No questions] "are of greater importance for the embryologist than those which concern the nature of the secondary changes likely to occur in the ftal or in the larval states; since it is on the answer to such questions that our knowledge of the extent to which a record of the ancestral history may be expected to be preserved in development depends" (Balfour, 1880–1881, vol. 2, p. 381
Balfour also expended considerable effort on larvae and larval evolution.
In the late 19th century, naturalists identified a vast diversity of marine larvae in plankton samples. How could this diversity be rationalized? What did it reveal about animal relationships and origins? One way to capture the flavor of the important position assigned to larvae at that time is to see how they were treated by Balfour in his Treatise; see the quotation above. To paraphrase his discussions of the "Department of Phylogeny," Balfour saw the aims of embryological research as:
- testing how far comparative embryology can reveal ancestral forms common to the whole of the Metazoa;
- revealing whether a particular embryonic larval form is constantly reproduced in the ontogeny of different animals, and whether that form represents the ancestral type of those groups;
- determining whether larval forms agree with living or fossil adults, an agreement that would imply that the adults were closely related to the parent stock of the group in which the larval form occurs;
- understanding how some organs can atrophy or become functionless in some groups but persist in others; and
- determining to what extent organs in development pass through a condition permanent in some lower form.
Today many assume that 19th-century embryologists all followed von Baer and Haeckel in regarding early development as immutable—as not subject to any change either ontogenetic or phylogenetic. This assumption is incorrect; a number of German embryologists saw early development as subject to change. Indeed, a number, including Balfour, Wilhelm Roux and August Weismann, perceived the hand of natural selection early in embryonic stages:
The principles which govern the perpetuation of variations which occur in either the larval or the foetal state are the same as those for the adult state. Variations favorable to the survival of the species are equally likely to be perpetuated, at whatever period of life they occur, prior to the loss of the reproductive powers. (Balfour, 1880–1881, vol. 2, p. 381
Balfour's perceptive view of natural selection, survival of the fittest, and inheritance of variation was specifically addressed in his vice-presidential address to Section D of the BAAS in August 1880 (Balfour, 1880b): Only the most favorable variations persist and they persist as secondary changes and adaptations in larvae. This view was echoed by Walter Garstang in his presidential address to Section D 40 yr later: "on the whole a larval evolution has taken place more or less parallel to that of the adult evolution, but subject to conspicuous deviations" (Garstang, 1929, p. 77).
Balfour emphasized variation of yolk content in closely related species, the effect of yolk content on the mode of cleavage, and suppression of developmental stages in fresh-water species and their retention in marine species as providing evidence for selection on early developmental stages. In the absence of a larval stage, development is likely to be abbreviated, direct, and associated with increased amounts of yolk in the egg. Balfour even used the term ‘direct development’ for ontogeny from which the larval stage has been lost, and argued that development that includes a larval stage is more likely to repeat ancestral history than is direct development because abbreviation obscures ancestral life history more than does secondary adaptation, or as Balfour expressed it: "There is a greater chance of the ancestral history being lost in forms which develop in the egg; and masked in those which are hatched as larvae" (1880–1881, vol. 2, p. 383).
Balfour sought to understand which larval types most resemble the ancestors of the phyla. To this end he distinguished two kinds of larvae: primary larvae (the Planula as the ancestral form of coelenterates) as modified ancestral forms that have existed as free larvae "from the time when they constituted the adult form of the species" (1880–1881, vol. 2, p. 383); and secondary larvae, introduced secondarily into the life history of species that previously developed directly. Secondary larval adaptations arose from changes in larval life or from changes in the order of appearance of structures, or were related to the struggle for existence.
Balfour's phylogenetic conclusions hinge on the central notion that groups that share a common larval type are "descended from a common stem" (1880–1881, vol. 2, p. 405). Common larval types are used to deduce a radially symmetrical, medusa-like organism as the common ancestor for all animal groups above coelenterates, i.e., for all triploblastic animals. As far as Balfour was concerned, this was the way embryology would unravel phylogenetic relationships, ancestors, and evolutionary history:
The majority of these conclusions are undoubtedly of a highly speculative character, but while they cannot be regarded as part of our stock of embryological knowledge, they may, nevertheless, serve to indicate an important line for continued embryological research. A thorough histological investigation of the larval forms dealt with in this essay will be likely to lead to valuable results. (1880–1881, vol. 2, p. 407)
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Young Archi-mollusks went to sea with nothing but a velum— A sort of autocycling hoop, instead of pram—to wheel ‘em; And, spinning round, they one by one acquired parental features, A shell above, a foot below—the queerest little creatures. (The Ballard of the Veliger or How the Gastropod got its Twist)
Walter Garstang (1868–1949) was educated at Oxford as evolutionary embryology was waning and experimental embryology was on the rise. Much of his career was spent in marine biology and in fisheries research on the staff of the Plymouth Laboratory, as director of the English North Sea investigations into fisheries research and finally as Professor of Zoology at Leeds University. The bulk of his writing was on larval biology and fisheries science, supplemented by wonderful verses (see the example above) written throughout his career but not published until 1951. These verses, his enormous sense of fun, a damaging tendency for theoretical speculation, and views that threatened the orthodoxy of Haeckel's theory of recapitulation, meant that the four papers Garstang wrote on the relationship between embryology and evolution, although now seen as his lasting legacy, received little attention during his lifetime.
For Garstang larval and adult evolution could occur independently, ancestry was to be found in larval and not in adult stages, but many larval features were secondary adaptations to larval life and so lacked phylogenetic information. Furthermore, organs must be retained in a functional state to allow free and independent larval existence (see Hall and Wake, 1999). In Garstang's day, as in Balfour's, many still followed Haeckel's Biogenetic Law: evolution occurs in adults not in larvae or embryos; the new stages are affixed to the end of the ancestral ontogeny; adaptation is limited to adult stages. In The Science of Life, for example, H. G. Wells wrote that "Tens of thousands of animals do recapitulate the past during their development ...and in none of these tens of thousands of cases is this departure intelligible save on the view that in so doing they are repeating phases that were once final forms in the earliest evolution of the race" (Wells et al., 1934, p. 369).
In speeches, papers (Garstang, 1922) and in verse, Garstang argued against Haeckel's Biogenetic Law and against contemporary recapitulationists such as Ernest MacBride, for whom invertebrates represented "those branches of the Vertebrate stock, which, at various times, have deserted their high vocation and fallen into lowlier habits of life" (1914, p. 662).
Larvae and vertebrate origins
In the 19th century, the two major rival theories of vertebrate origins used either embryological evidence to argue that the ascidian tadpole was the closest living representation of the common vertebrate ancestor, or adult morphology to argue that a segmented annelid or proto-annelid gave rise to vertebrates and arthropods (see Ghiselin, 1994; Maienschein, 1994; Nübler-Jung and Arendt, 1994; Bowler, 1996; Gee, 1996, and Hall, 1996 for discussions). In 1866, Haeckel introduced the concept of caenogenesis to cover those situations in which recapitulation of phylogeny in ontogeny was obscured because of larval adaptations or the displacement of embryonic or larval stages in time or space during ontogeny. We retain the term, but modern usage tends to follow de Beer, who in turn followed Garstang in restricting caenogenesis to larval adaptations, without any reference to recapitulation.
According to Garstang, larvae acted as agents of dispersal, like the seeds of plants. Any reduction of the free-swimming larval stage was a secondary consequence of retention of larvae within the female. Modification or loss of the larval stage (as seen in direct development) demonstrated the plasticity and adaptability of ontogeny and ontogenetic stages. Garstang argued that although many larval features were secondary adaptations to larval life, ancestry should be sought in larvae not in adults and that, contrary to Haeckel, ontogeny creates phylogeny, it does not recapitulate it: "Many have been the attempts to find the evolutionary history of the vertebrates, but it was reserved for the late Professor Garstang to put forward the only theory which is free from the most crude objections" (de Beer, 1962, p. 63).
Although Garstang's first published volley against the Biogenetic Law was in an address to the Linnean Society in 1922 (in which he coined the now famous phrase "ontogeny does not recapitulate phylogeny: it creates it," p. 81), his ideas were fully worked out earlier. At a lecture around Easter 1920, he argued that planktonic larvae are specialized larval adaptations and not primitive and ancestral adult types, emphasized the competing selective advantages of providing the basis for the adult while acting to distribute the species, and stresses that selection acts as powerfully on young as it does on adult stages (Hardy, 1951, pp. 4–5). Garstang's second and third presentations were the 1928 presidential address to Section D (Zoology) of the BAAS and a 1929 paper on the relationship of tunicates to chordate phylogeny. His last publication on the subject (in 1946) was on the morphology and relationships of the Siphonophora.
Garstang demonstrated the incompatibility of the Biogenetic Law with Mendelian genetics, showed that larvae could influence the course of evolution, and used the origin of torsion in gastropods and the transformation of Tornaria larvae to show that the evolution of new features was based in alteration of ontogeny, not modification of adults. He (1928) used his own remarkable comparisons of larval echinoderms and early chordate embryos (1894, 1896) to propose the revolutionary theory that vertebrates arose from some "proto-echinoderm" through a process of paedomorphosis and neoteny, the echinoderm larva becoming, in effect, an adult chordate (tunicate). Ascidians were not degenerate chordates but represented the primitive chordate condition with planktonic larvae. Garstang envisaged the chordate ancestor as a sessile invertebrate rather like an ascidian with planktonic larvae, selection acting on the larvae to promote dispersal via evolution of a muscular tadpole-like tail, accelerated development of the gonads through neoteny so that the prolonged larval stage became sexually mature while still planktonic (as the axolotl does while still aquatic), allowing the sessile, bottom-living adult to be eliminated and the active larva to become a free-living adult.
Thus upstart, lively, sexually precocious larval novelties, not ancient sessile adults, set the stage for evolution. In the words of Alister Hardy, "Garstang, with his concept of paedomorphosis, has altered our whole outlook on the process of evolution" (1951, p. 15). Indeed, Garstang laid the basis for many of the topics that occupy us today—life history evolution, the ancestry of the vertebrates, phylogenetic relationships between the animal phyla, relationships between macro- and microevolution, developmental constraints, modification of ontogeny during evolution, origin of novelties, and so forth.
What evolutionary mechanism could bring about such dramatic changes? Gavin de Beer recognized the critical importance of paedomorphosis; coined a companion term, gerontomorphosis, for evolutionary changes brought about by modification of adult structures; and provided a mechanism in heterochrony.
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By delaying its processes of development, an animal can, as it were, fail to grow up.... I believe that this Peter-Pan type of delayed development has been of the greatest importance in the evolution of animals. (BBC Science Survey Broadcast, 19 September 1950; de Beer, 1962
Sir Gavin de Beer (1899–1972) was perhaps the last of the grand comparative anatomists and evolutionary embryologists whose breadth, output and skills as an expositor spanned the interests and aptitudes of the likes of Lankester and Huxley. Arguably the greatest descriptive embryologist of his generation, de Beer, educated at Oxford was successively Jenkinson Lecturer in Embryology at Oxford, Professor of Embryology at University College, Director of the British Museum (Natural History 1950–1960) and a director of Thomas Nelson, Publishers.
De Beer made major contributions to our understanding of head segmentation (to which topic Balfour had contributed much), skull development, and the pituitary gland. His comparative vertebrate anatomy was grounded in embryology. This was not experimental embryology, although de Beer was trained in experimental methods (studying tissue culture with Strangeways in Cambridge and techniques of embryo surgery with Spemann in Germany). He wrote books on growth and genetics and an important text on experimental embryology with Julian Huxley. de Beer did detailed comparative embryology using large-scale wax and plaster of Paris models based on serially sectioned embryos, reminding us of Balfour's use of serial sections. On a broader canvas, chiefly through the books Embryology and Evolution (1930), Embryos and Ancestors (1954) and Atlas of Evolution (1964).8 de Beer sought to unite evolution and embryology through a mechanistic explanation for structural evolution in heterochrony and to separate homology from the strait jacket imposed by the germ-layer theory and by strict embryological criteria.
Heterochrony
De Beer's contribution to evolutionary embryology through the development of a theory of heterochrony (‘Peter-Pan evolution; see the epigraph) is well known. Perhaps less well known is that de Beer was one of the first to integrate genetics into evolutionary embryology, incorporating into heterochrony Richard Goldschmidt's findings on genes that effect rates of developmental processes (discussed in this issue by Dietrich).
By acting at different rates, the genes can alter the time at which certain structures appear...This conclusion ...enables us to see how changes and indeed reversals in the order of development of structures can take place...To this phenomenon the term heterochrony may be applied (de Beer, 1954
De Beer saw the genetic and evolutionary advantages that would accrue to organisms when heterochrony resulted in paedomorphosis:
A species undergoing paedomorphosis will find itself in possession of a number of genes whose functions were to control characters which no longer appear, since the old adult characters will be lost in neoteny, and old structures will be replaced by new ones in deviation. It is, therefore, possible to imagine that these ‘unemployed’ genes are available for new variation, and that paedomorphosis may contribute directly to an increase of genetic and evolutionary plasticity in this way (1954, p. 93).
He summarized his conclusions concerning heterochrony thus:
- Qualitative evolutionary novelties can and do appear at all stages in ontogeny, and not solely in the adult.
- Characters can and do change the time and order of their appearance in the ontogeny of the descendant as compared with that of the ancestor.
- Quantitative differences between characters. resulting in heterochrony, play a part in phylogeny in addition to the introduction of qualitative novelties.
- The different characters of an organism do not necessarily all evolve by the same mode (de Beer, 1954, p. 88).
Homology
De Beer was also especially concerned with the criteria used to determine homology, publishing his most influential ideas in a slim "pamphlet" (1971) that laid the basis for the views that many of us hold today. This emphasis on homology brings us back to the issues that preoccupied Balfour a century earlier. de Beer argued that, for determining homology, the embryonic stages when organ rudiments and relationships among organs are well established may be useful but earlier stages are not. Balfour had taken the opposite view. In particular, de Beer dismissed origin in common germ layers, origin by the same inductions, and origins from a common genetic basis as necessary criteria for homology; see Hall (1995) for detailed analysis.
Concerning constancy of germ layer of origin, de Beer concluded that: "correspondence between homologous structures cannot be pressed back to similarity of position of the cells of the embryo or the parts of the egg out of which these structures are ultimately differentiated" (1971, p. 3). For example, the alimentary canal in different classes of vertebrates forms from different germ layers associated with the archenteron while cartilage and bone arise from both ectoderm (neural crest) and mesoderm in the axolotl, Ambystoma, a dual origin that de Beer thought was true for all vertebrates.
Concerning the requirement for commonalty of inductive mechanism, he concluded that "homologous structures can owe their origin and stimulus to differentiate to different organizer–induction processes without forfeiting their homology" (de Beer, 1971, p. 13). Among the examples cited is induction of the lens by the optic cup in Rana fusca but not in the congeneric species R. esculenta.
Concerning the need for a shared genetic basis for structures to be homologous, de Beer analyzed phenocopies, homeotic mutants and the eyeless (ey) gene in Drosophila to conclude that: "characters controlled by identical genes are not necessarily homologous...Therefore, homologous structures need not be controlled by identical genes, and homology of phenotypes does not imply similarity of genotypes" (de Beer, 1971, p. 15).
de Beer's analyses of the relationship between homology and embryology have stood the test of time. Variations in germ layer of origin, developmental processes or genetic basis, need not render structures non-homologous. Conversely, shared germ layers, developmental processes or genetic bases do not guarantee that two structures are homologues (Hall, 1995, 1998b). So, at the end of the first century of evolutionary embryology (de Beer, 1971) as at the beginning (Balfour, 1873a), considerations of homology remained central to any understanding of the relationship between embryology and evolution. They still do.
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ACKNOWLEDGMENTS |
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Research support from NSERC (Canada) and the Killam Trust of Dalhousie University is gratefully acknowledged as is the editorial expertise of June Hall.
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1 From the Symposium Evolutionary Developmental Biology: Paradigms, Problems, and Prospects presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
3 Allman (1853) named the outer and inner layers ectoderm and endoderm; Huxley (1849) coined the term mesoderm for the middle layer.
4 This whole enterprise fell apart in the 1880s, but I am dealing with the origins, not the demise, of evolutionary embryology, for which see Bowler (1996), Gee (1996) and Hall (1996, 1998b).
5 For simplicity and to avoid confusion, when discussing Balfour's work I usually use the terms ectoderm, endoderm and mesoderm for epiblast, hypoblast and mesoblast.
6 According to the fin-fold theory proposed by Thacher (1877), Mivart (1879) and Balfour (1881), and therefore known as the Thacher–Balfour or Thacher–Mivart–Balfour fin-fold theory, paired fins share common elements with the median unpaired fins in that both are derived from folds of the body wall and supported by skeletal elements; see Hall (1991) for an evaluation.
7 This was not Balfour's last word on germ layers. He revisited them in the embryonic chick with his student F. Deighton (Balfour and Deighton, 1882). However, this study added little to Balfour's descriptions published in 1873.
8 Embryos and Ancestors is an updated revision of Embryology and Evolution. de Beer's productivity was enormous. In addition to 382 papers and articles, he wrote 16 books in zoology, evolution, embryology and growth; five books on the history of science; nine biographical books (including important studies on Darwin that included a reprint of the sixth edition of the Origin of Species, the last edition to appear during Darwin's lifetime); nine books on Switzerland; and six books on military and other topics.
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SYNOPSISINTRODUCTIONBALFOUR: COMPARATIVE AND...GARSTANG: PAEDOMORPHOSIS AND...DE BEER: HETEROCHRONY AND...References |
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Allman, G. J. 1853. On the anatomy and physiology of Cordylophora: A contribution to our knowledge of Tubularian zoophytes. Phil. Trans. R. Soc. Lond. B, 143:367-384.
Baer, K. E. von. 1828. Über Entwicklungsgeschichte der Thiere.. Beobachtung und Reflexion. Gebrüder, Bornträger, Königsberg.
Balfour, F. M. 1873a. The development and growth of the layers of the blastoderm. Q. J. Microsc. Sci, 13:266-276.
Balfour, F. M. 1873b. On the disappearance of the primitive groove in the embryo chick. Q. J. Microsc. Sci, 13:276-280.
Balfour, F. M. 1873c. The development of the blood vessels of the chick. Q. J. Microsc. Sci, 13:280-290.
Balfour, F. M. 1874. A preliminary account of the development of the elasmobranch fishes. Q. J. Microsc. Sci, 4:323-364.
Balfour, F. M. 1878. A monograph on the development of elasmobranch fishes.. Macmillan & Co., London.
Balfour, F. M. 1880a. On the structure and homologies of the germinal layers of the embryo. Q. J. Microsc. Sci, 20:247-273.
Balfour, F. M. 1880b. Vice-Presidential address before the Anatomical and Physiological section of the British Association at Swansea, August 27 1880. "Embryology and the Darwinian theory," Brit. Assoc. Report, 1880:636-644[Also published in Nature 22:417–420].
Balfour, F. M. 1880–1881. A treatise on comparative embryology.. Two Volumes. Macmillan & Co., London.
Balfour, F. M. 1881. On the development of the skeleton of the paired fins of Elasmobranchii, considered in relation to its bearing on the nature of the limbs of the Vertebrata. Proc. Zool. Soc. Lond, 1881:656-671/LPAGE>.
Balfour, F. M., and F. Deighton. 1882. A renewed study of the germinal layers of the chick. Q. J. Microsc. Sci, 22:176-186/LPAGE>.
Bateson, W. 1922. Evolutionary faith and modern doubts. Science, 55:53-61.
de Beer, G. R. 1930. Embryology and evolution.. Clarendon Press, Oxford.
de Beer, G. R. 1954. Embryos and ancestors.. Revised edition. Clarendon Press, Oxford.
de Beer, G. R. 1962. Reflections of a Darwinian.. Essays and addresses. Thomas Nelson and Sons Ltd., London.
de beer, G. R. 1964. Atlas of evolution.. Thomas Nelson & Sons, London.
de Beer, G. R. 1971. Homology: An unsolved problem.. Oxford Biology Reader No. 11, Oxford University Press, London.
Bowler, P. J. 1996. Life's splendid drama.. Evolutionary biology and the reconstruction of life's ancestry 1860–1940. The University of Chicago Press, Chicago, IL.
Garstang, W. 1894. Preliminary note on a new theory of the phylogeny of the Chordata. Zool. Anz. 17:122–125Q. J. Microsc. Sci, 72:51-54.
Garstang, W. 1896. The origin of vertebrates. Proc. Camb. Phil. Soc, 9:19-47.
Garstang, W. 1922. The theory of recapitulation: A critical restatement of the Biogenetic Law. Proc. Linn. Soc. Lond. Zool, 35:81-101.
Garstang, W. 1928. The morphology of the Tunicata and its bearing on the phylogeny of the Chordata. Q. J. Microsc. Sci, 72:51-54/LPAGE>.
Garstang, W. 1929. The origin and evolution of larval forms. British Association for the Advancement of Science, Rep. 96th Meet. pp. 77–98.
Garstang, W. 1946. The morphology and relations of the Siphonophora. Q. J. Microsc. Sci, 87:103-197.
Gee, H. 1996. Before the backbone: views on the origin of the vertebrates.. Chapman & Hall, London.
Ghiselin, M. T. 1994. The origin of vertebrates and the principle of succession of functions. Genealogical sketches of Anton Dohrn 1875. An English translation from the German, introduction and bibliography. Hist. Philos. Life Sci, 16:3-96.[Medline]
Haeckel, E. 1866. Generelle Morphologie der Organismen, Vols. 1 & 2. Berlin.
Hall, B. K. 1991. Evolution of connective and skeletal tissues. In J. R. Hinchliffe, J. M. Hurle and D. Summerbell (eds.), Developmental patterning of the vertebrate limb, NATO ASI Series A, Life sciences, Vol. 205, pp. 303–311. Plenum Press, New York.
Hall, B. K. 1995. Homology and embryonic development. Evol. Biol, 28:1-37.
Hall, B. K. 1996. Baupläne, phylotypic stages, and constraint: Why are there so few types of animals? Evol. Biol, 29:215-261.
Hall, B. K. 1998a. Germ layers and the germ-layer theory revisited: Primary and secondary germ layers, neural crest as a fourth germ layer, homology, demise of the germ-layer theory. Evol. Biol, 30:121-186.
Hall, B. K. 1998b. Evolutionary developmental biology.. 2nd ed. Kluwer Academic Publishers, Dordrecht, Netherlands.
Hall, B. K. 1999a. The neural crest in development and evolution.. Springer-Verlag, New York.
Hall, B. K. 1999b. The paradoxical platypus. BioScience, 49:211-218.
Hall, B. K. 2000. The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic. Evol. & Devel, 2:1-3.[Medline]
Hall, B. K., and M. H. Wake. 1999. Introduction: Larval development, evolution and ecology. In B. K. Hall and M. H. Wake (eds.), The origin and evolution of larval forms, pp. 1–19. Academic Press, San Diego.
Hardy, A. C. 1951. Introduction. In W. Garstang, Larval forms and other zoological verses, pp. 1–21. Chicago University Press, Chicago.
Huxley, T. H. 1849. On the anatomy and the affinities of the family of the Medusæ. Phil. Trans. R. Soc, 139:413-434.
Lankester, E. R. 1873. On the primitive cell layers of the embryo as the basis of genealogical classification of animals, and on the origins of vascular and lymph systems, Ann. Mag. Nat. Hist. ser, 4:.11321-328.
Lankester, E. R. 1877. Notes on the embryology and classification of the animal kingdom: Comprising a revision of speculations relative to the origin and significance of germ layers. Q. J. Microsc. Soc, 17:399-454.
Lankester, E. R. 1878. Balfour on Elasmobranch Fishes. Nature, 18:113-115.
MacBride, E. W. 1914. Textbook of embryology, Vol. I, Invertebrates.. W. Heape (ed.) Macmillan & Co., London.
Maienschein, J. 1994. "It's a long way from Amphioxus." Anton Dohrn and late nineteenth century debates about vertebrate origins. Hist. Phil. Life Sci, 16:465-578.
Mivart, St. G. 1879. On fins of Elasmobranchs. Trans. Zool. Soc. Lond, 10:1-76.
Nübler-Jung, K., and D. Arendt. 1994. Is ventral in insects dorsal in vertebrates? A history of embryological arguments favouring axis inversion in chordate ancestors. Roux's Arch. Devel. Biol, 203:357-366.[CrossRef]
Pander, C. H. 1817. Dissertatio inauhuralis, sistens historiam metamorphoseos quam ovum incubatum prioribus quinque diebus subit. Würzburg.
Rathke, M. H. 1825. Flusskrebs. Isis von Oken, Jahrb, 2:1093-1100.
Sedgwick, A. 1894. On the inadequacy of the cellular theory and on the early development of nerves, particularly of the third nerve and of the sympathetic in Elasmobranchii. Q. J. Microsc. Sci, 37:87-101.
Thacher, J. K. 1877. Median and paired fins, a contribution to the history of vertebrate limbs. Trans. Connecticut Acad. Sci, 3:281-308Plates XLIX-LX.
Wells, H. G., J. Huxley, and G. P. Wells. 1934. The science of life.. The Literary Guild, New York.
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