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PALAEONTOLOGY AND EVOLUTIONARY DEVELOPMENTAL BIOLOGY: A SCIENCE OF THE NINETEENTH AND TWENTY-FIRST CENTURIES by

BRIAN K. HALL

ABSTRACT. A wind of change has swept through palaeontology in the past few decades. Contrast Sir Peter Medawar's dismissive: `palaeontology is a particularly undemanding branch of science' (as recalled by John Maynard Smith in Sabbagh 1999, p. 158) with `Palaeontology: grasping the opportunities in the science of the twenty-®rst century', the title of a contribution to a special issue of Geobios by the Cambridge palaeontologist, Simon Conway Morris (1998a). The winds of change have come partly from palaeontologists seeking to broaden the impact of their studies and partly from biologists (neontologists) realizing the contributions that palaeontology can make to their disciplines. Consequently, impressions of past life preserved in stone are coming alive. Fossils are being described and analyzed using new tools and languages as the static fossil record becomes a record of transitions in patterns that can be explained and related to biological, ecological, climatic and tectonic changes. The latest addition is evolutionary developmental biology, or èvo-devo', whose language provides a new basis upon which to interpret anatomical change, both materially and mechanistically. In this review I examine the major contributions made by palaeontology, how palaeontology has been linked to evolution and to embryology in the past, and how links with evo-devo have enlivened and will continue to enliven both palaeontology and evo-devo. Closer links between the two ®elds should illuminate important unresolved issues related to the origin of the metazoans (e.g. Why is there a con¯ict between molecular clocks and the fossil record in timing the metazoan radiation; were Precambrian metazoan ancestors similar to extant larvae or to miniature adults?) and to diversi®cation of the metazoans (e.g. How do developmental constraints bias the direction of evolution; how do microevolutionary developmental processes relate to macroevolutionary changes?). KEY WORDS:

palaeontology, evolution, development, evolutionary-development biology, embryology, neural crest.

`The evolution of organisms must really be regarded as the evolution of developmental systems' (Waddington 1975, p. 7) P A L A E O N T O L O G Y is the study of life from the past. Evolutionary developmental biology (or evo-devo as it is colloquially known) is the study of how development has evolved and how modi®cations of development affect evolutionary change (Raff 1996; Hall 1999; Hall and Olson in press). The editors of Palaeontology invited an overview of why palaeontology needs evolutionary developmental biology. More speci®cally, the request was `to write an article on `why palaeontology needs (or should be interested in) evo-devo', along the lines of Conway Morris' `why molecular biology needs palaeontology' but from the opposing view point'. At ®rst glance, my remit may seem odd. Why should those who study extinct (usually adult) animals be concerned about the science of embryos and embryonic development? [Palaeontology, of course, includes the study of extinct plant life, and the study of trace fossils (trackways, bite or tooth marks, impressions of skin, and so forth), but I am con®ning my comments to animals]. What could evo-devo possibly offer palaeontologists as they go about their daily tasks? I trust that by the end of this review, the conceptual advances and deeper understanding of mechanisms that ¯ow from a tighter integration of palaeontology and evo-devo will be evident. As there are long links between the three ®elds, I place the discussion in the context of how palaeontology related to evolution and to embryology in the past. This includes the in¯uence of evolutionary embryology (the predecessor of evo-devo) on palaeontology in the nineteenth century, the application of `laws of construction' and the rise of palaeobiology in the twentieth century. I then discuss more recent links between palaeontology and evo-devo, drawing examples primarily from studies on vertebrates. This undoubted bias in part re¯ects my [Palaeontology, Vol. 45, Part 4, 2002, pp. 647±669]

q The Palaeontological Association

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PALAEONTOLOGY, VOLUME 45

greater familiarity with vertebrates. But it re¯ects a deeper issue of limited interactions between evolutionary developmental biologists interested in body-plan evolution and invertebrate palaeontologists. It is not that we lack studies on the relationships between the invertebrates. It is the origins of the invertebrate phyla that are more different to access palaeontologically than are those of the vertebrate phyla. A recent approach is Budd's (2001) attempt to tie the patterns of the evolution of segmentation in arthropods to the evolution of development; also see Budd and Jensen (2000). One individual who saw the links was Conrad Waddington. Although he spent his career synthesizing genetics, embryology and evolution, Waddington, one of the `developmental evolutionists' to use Arthur's (1988) phrase, began as a palaeontologist. He chose ammonites to study because their shells recorded the developmental processes responsible for evolutionary changes in shell morphology. His conviction `that the evolution of organisms must really be regarded as the evolution of developmental systems' (Waddington 1975, p. 7) could serve as the prescient motto for evo-devo and palaeontology. Another who sees the future links is Henry Gee: If I could pick a research area for palaeontologists, it would be evolutionary developmental biology, in which palaeontologists contribute to the general aim of elucidating the origins of morphological novelty ± working alongside molecular developmental biologists and geneticists (Gee 2001, p. 62). PALAEONTOLOGY AND EVOLUTION

Georges Cuvier is rightly regarded as à paleontologist, perhaps the ®rst to deserve the name' (Coleman 1964, p. 114). However, palaeontology existed before there were palaeontologists. Many earlier writers described fossils, but the term `fossil' was used for any object dug out of the ground (Rudwick, 1985). Konrad Gesner, for example, who, from 1551 on, compiled an encyclopaedia of all animals (Historia Animalium) that ran to 4500 pages, produced, in 1565, a beautifully illustrated compendium of all `fossils' that included stones and gems. Indeed, Rudwick (1985) dated the history of palaeontology from the 28th of July, 1565, the day that Gesner ®nished his book. Gesner, who died several months later in Vienna of the plague, compared fossils with extant organisms which they resembled (a fossil `crab' with Pagurus, a living crab, but also compared objects such as Glossopterae (tongue-stones) with the teeth of living sharks, ®guring both the tongue stone and the shark to scale in the same plate. Colonna (1616) and subsequently Steno (see Rudwick, 1985) showed that tongue stones were indeed teeth of large sharks. Gesner entertained various theories of the nature of the fossil objects he described: the remains of animals that once lived; ideal types of animals that never were alive; a trick (of God?) to disturb the natural order; a test of one's faith in God. The origins of palaeontology as a science may be traced to the con®rmation by Cuvier in the early part of the nineteenth century, that impressions seen in stones were traces of organisms that lived in the past, species removed from the earth by extinction. Palaeontology became the zoology and botany (and later the biology) of organisms of the past and a branch of comparative morphology (Haber 1959; Rudwick 1985, 1997; Young 1992). Cuvier's ability to reconstruct extinct animals from a few skeletal elements, to reconstruct the muscular system from muscle scars preserved on bones, and to assign specimens to genus and species from a single bone, was legendary. Following Cuvier, nineteenth century morphologists such as Richard Owen, Thomas Henry Huxley, William Buckland and Edward Forbes Jr described fossils [especially dinosaurs, other `reptiles' (archosaurs) and Archaeopteryx] as they would describe the anatomy of living animals. They were especially concerned with transitions between major groups of animals, such as between reptiles and birds (Owen 1863, 1870; Huxley, 1868, 1870; see Ospovat 1976, 1995). Owen was known as the `British Cuvier', although this title, or the Ènglish Cuvier', or the `next Cuvier', also was applied to the anatomist Robert Grant and to the palaeontologist Gideon Mantell (Desmond 1979; Cadbury 2000). The fascination among the public in the United Kingdom for fossils can be traced to an amateur, although a very professional àmateur', Mary Anning of Lyme Regis, who discovered the ®rst British ichthyosaur in 1812 when she was 12. Subsequent discoveries of the ®rst plesiosaur in 1824 (which she sold to the Duke of Buckingham for £200) and the ®rst British pterosaur in 1828 (which she took ten years to excavate) cemented her reputation, a fascination for fossils in the British public, and provided specimens for which the professionals actively competed in their quest to describe and understand fossils

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(Blair 1975; Cadbury 2000). At least one novel, Dragon in the Cliff (Cole 1991), is based on Mary Anning's life. Nowadays, it is taken for granted that palaeontology is an evolutionary science, changes in fossils over time re¯ecting evolutionary changes in past organisms and in their environments. This was not always so. Whereas fossils were accepted as evidence of past life forms and their progress through the ages, they were not so readily accepted as providing evidence for continued improvement or progress toward perfection of life on the planet; not that progress necessarily implies evolutionary progress. We may look to the anniversary lecture delivered in 1851 by Charles Lyell to one of the most prestigious scienti®c societies then in existence, the Geological Society of London. Lyell marshalled 12 principal points against the notion that the fossil record provides evidence for progression of life forms. His points included some rather telling pieces of evidence against progressivism: 1, the earliest fossil plants were not the simplest plants known; 2, these early plants were found in marine deposits and so provided no information concerning the land ¯ora; 3, the oldest Silurian strata contained highly developed examples of major groups of invertebrates; 4, the record of fossil ®sh showed no clear evidence of increasing organization with time; 5, fossil reptiles were present in the Carboniferous, and so on. Lyell was writing before the publication of On the origin of species, a book that transformed the interpretation of the fossil record. Thomas Huxley, although he was well aware of Darwin's developing ideas, was a rather unwilling participant in the transformation of thinking and a reluctant palaeontologist. When offered the opportunity to replace Edward Forbes as Palaeontologist and Lecturer on Natural History at the Royal School of Mines in 1854, Huxley refused the position of palaeontologist because he `did not care for fossils' (L. Huxley, 1900, vol. 1, p. 132). He published 38 papers on fossils between 1856 and 1871, not a bad record for someone who did not care for them. Huxley saw evidence for evolution in the fossil record, declaring in an address before the British Association for the Advancement of Science at York in September, 1881 that `the palaeontological discoveries of the last decade are so completely in accord with the requirement of this [the evolution] hypothesis, that, if it had not existed, the palaeontologist would have had to invent it' (cited in L. Huxley 1900, vol. 2, p. 34). So, by the 1880s, palaeontology was an evolutionary science. Indeed, Ospovat (1995, p. 140) believed that `there may be more than a grain of truth in Huxley's unintentional suggestion that the course of paleontology was on by the 1840s would have established the doctrine of descent even without the Origin' Palaeontology also was much in¯uenced by the embryology of the nineteenth century. PALAEONTOLOGY AND EMBRYOLOGY

Nowadays, palaeontology does not conjure up visions of a science steeped in embryology. Embryology however, has impinged on palaeontology in at least two fundamental ways: as a basis for palaeontological investigation, and through the provision of parallels and embryological `laws' against which fossils could be interpreted. Most of the zoological research undertaken in the latter part of the nineteenth century was embryological, morphological or palaeontological (Schuster and Shipley 1917; Coe 1918; Bowler 1984, 1996). Evolutionary embryology, which sought to unravel the relationships between and the origins of the major groups of extant, but also, where appropriate, fossil animals using comparative embryological evidence, drove much of the research in zoology (Hall 2000a), while embryology and embryological theory provided fundamental underpinnings for much of the palaeontological research. Coe and Rudwick offered two visions of the links between embryology and palaeontology: The morphological, embryological and paleontological evidences of evolution as indicated by homologies, developmental stages and adaptations were the most absorbing subjects of zoological research and discussion. (Coe 1918, p. 412, speaking of the period 1870±1890 in America) Throughout the nineteenth century the conceptual links between embryology and palaeontology provided a fertile source of analogies. This is re¯ected in the use of the same terms (evolution, development, Entwicklung, etc.) to

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describe directional change in organisms, both in embryonic growth and in geological time... Both sciences were concerned with understanding the process of coming-into-being of organisms; both, on different levels, faced the problem of explaining the emergence of diversity and novelty in organic form and function during the passage of time ± whether the short time-scale of an individual life-history or the immensely long time-scale of the fossil record. (Rudwick 1985, p. 225)

As evidenced by his Hunterian lectures of 1841, Richard Owen was an early British adherent to von Baer's embryological law. Just as von Baer saw embryos progressing from general to speci®c forms, Owen saw fossils as more likely to provide general forms and features, with extant species providing more speci®c forms (Ospovat 1976, 1995; Richards 1987; Desmond 1982, 1985, 1989; Rupke 1994). Embryologists also saw links between embryos and fossils. For example, Meckel (1811, 1821) proposed a parallelism between stages in human development and the adult stages of other vertebrates. We are in turn ®sh, reptile, non-human mammal, and only ®nally human, Meckel argued. For Meckel, the same developmental force controlled individual development (ontogeny) and changes in organisms over time (phylogeny). A parallel between these developmental stages and the appearance of life as seen in the fossil record did not escape his attention. Embryologists sought ancestors in embryos, interpolating missing stages (complete with names and invented descriptions) wherever there were gaps that embryonic stages could not ®ll (Hall 2000a). For example, Balfour (1881) proposed the `Proto-Gnathostomata' as a hypothetical (but necessary) group in the lineage leading to the chordates. Protognathostomes had branchial skeletal elements, one of which, the mandibular, was subsequently converted into the jaw skeleton of the ®rst gnathostome. Interpolating hypothetical groups persisted as an approach for many decades. In 1933, the Cambridge zoologist and ichthyologist Hans Gadow still saw `that these [the Proto-Gano-Dipnoi], to the exclusion of all other ®shes, represented the ancestral stage of all Gnathostomata.' (1933, p. 66, note 1) Palaeontologists, whose discipline was fundamentally, if not entirely, based on morphology, marched to the same drum. If transitional forms were not present in the fossil record, they used the embryological approach to compensate for the inadequacies of an incomplete fossil record, or invoking types, such as Agassiz's (1850) prophetic type, that combined features found separately in later forms (Ospovat 1995). Consequently, many palaeontologists saw the parallel between individual development and the evolutionary history of a group as an evolutionary mechanism, and evolutionary morphology persisted longer in palaeontology than in any other ®eld of science (Ospovot 1995; Bowler 1996). This is illustrated well by palaeontology in America in the late 1800s and early 1900s. PALAEONTOLOGY IN AMERICA

An appreciation of the unidirectional vector of embryonic development had a profound in¯uence on palaeontology; almost all of the most in¯uential American palaeontologists practising in the late nineteenth and early twentieth centuries adhered to orthogenesis (linear trends in evolution, driven by internal factors rather than by natural selection), analogous to the ordered trends seen in embryonic development (Lull 1918; Ruse 1996). Trenchant as ever, G. G. Simpson described this view as à product rather of the tendency in the minds of scientists to move in straight lines than of a tendency for nature to do so' (1944, p. 164). The list of adherents included Edward Drinker Cope (mammalian evolution), Alpheus Hyatt (ammonites) and Henry Fair®eld Osborn (vertebrate palaeontology). They wrote books with titles such as The origin of the ®ttest and The primary factors of organic evolution (Cope 1887, 1904), and From the Greeks to Darwin (Osborn 1894), wherein we ®nd such statements as: Examination of all these genealogical lines reveals a certain de®niteness of end and directness of approach. We discover no accessions of characters which are afterwards lost... Nor do we discover anything like the appearance of sports along the line...On the contrary...progressive evolution has advanced by minute increments along a de®nite line,... variations off this line have not exerted an appreciable in¯uence on the result. (Cope 1887, pp. 149±150)

These individuals followed trends such as increase in mean body size during the history of a lineage (Cope's law), or the inexorable increase in the size of organs with body size [as seen in the horns on titanotheres (Osborn 1915) or the antlers on the Irish elk] with the belief that `certain tendencies of evolution may carry a phylum beyond its requirements in adaptation' (Osborn 1929, p. 28).


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Most were Lamarckians or neo-Lamarckians. Packard (1901), who with Cope and Hyatt founded the neo-Lamarckian school in America, discussed more than 40 palaeontologists who favoured some form of use/disuse rather than natural selection as the mechanism of evolutionary change. Such a mechanism is fundamentally embryological or epigenetic, as organisms develop in response to environmental cues. Hyatt's view of the evolutionary process is typical: èvolution is apparently a mechanical process in which the action of the habitat is the working agent of all the major changes' (Hyatt 1893, p. 374). Osborn's advocacy of a neo-Lamarckian version of orthogenesis, perhaps surprisingly, did not place him outside the evolutionary mainstream. We may believe that Lamarckism had few followers in the ®rst decades of the twentieth century, but according to a contemporary account, ìt still has a popular vogue that is widespread and vociferous' (Morgan 1916, p. 32). Palaeontologists who adhered to orthogenesis were not outcasts. Osborn and Bateson both spoke in a symposium organized by the American Society of Zoologists for their annual meeting in Toronto in December 1921, a symposium that examined orthogenesis as seen by the biochemist, geneticist, bacteriologist, zoologist and palaeontologist. Osborn also carried on an active correspondence with leading students of evolution from many camps, including William Bateson, Ray Lankester, E. P. Poulton, E. G. Conklin, C. B. Davenport, Julian Huxley, T. H. Morgan, G. G. Simpson and E. B. Wilson (Rainger 1980, pp. 10±11, and see Gerson 1973, and Rainger 1981, 1986 for Osborn's views on evolution). Orthogenesis may have been misguided, but embryology worked through orthogenesis to enliven palaeontology and evolutionary theory. Incorrect theories can, and perhaps often do, lead to appropriate outcomes. Although growth trends were analyzed and allometry was taken into account, paradoxically, variation did not ®t into the palaeontological world view of evolution and none took a population-level approach (Gerson 1973; Rainger 1985). Variation through time, rather than spatial variation, preoccupied palaeontologists. Many descriptions of new fossil species were based on single specimens, or even on portions of single specimens. The requirement to describe a holotype for new species focussed the attention of the palaeontologist onto type specimens. Without variation, unsurprisingly, there is nothing for selection to act upon. Consequently, natural selection had no explicit role to play in their view of evolution. Many may have assumed the operation of natural selection, and Osborn's was an attempt to chart trends in lineages that affect adaptations, i.e. to examine the effects of selection. By the Second World War this situation had changed, as can be seen in a passage from the major contribution made by a palaeontologist to the modern synthesis, Tempo and mode in evolution: ...the action of natural selection on intragroup (or interindividual) variations is essentially an originating force: it produces de®nitely new sorts of groups (populations), and the interbreeding group is the essential unit of evolution. (Simpson 1944, p. 31)

Jablonski (2000) summarized ways of teasing variation from the fossil record. Of course, response to selection need not involve structural changes that would be preserved in the fossil record, either because structural changes are not preserved or because both animals and plants can respond to climatic changes by moving to a new location, minimizing the effects of climatic change, but also minimizing the needs for structural adaptation. As examples of such palaeoecological analyses, see Davis and Shaw (2001) for adaptation of terrestrial plants to Quaternary climatic changes, Hellberg et al. (2001) for climate-driven range expansion in a marine gastropod in recent and Pleistocene times, and Vrba (1983) for range adaptation of African bovids to climate change. As a further indication of the in¯uence of embryology as the mechanism transferring use/disuse to evolutionary change, Cope postulated a growth force as an energy that ¯owed to parts that had been exposed to external stimuli (Davidson 1997). Horns appeared in adults in phylogenetically more basal titanotheres but developed early in ontogeny in later forms. Osborn interpreted this change as òntogenetic acceleration' gradually pushing horn development `forward into younger and younger ontogenetic stages until ®nally they [the horns] appear on the skull before birth' (Osborn 1929, pp. 814±815; see also Osborn 1915). (Genetic assimilation, by which features such as calluses on ostrich sterna, that are initially evoked in adults in response to environmental signals, subsequently arise in the embryos of descendants in the absence of the signal read-out of the genotype to-on is one possible mechanism for ontogenetic

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acceleration; Waddington 1957, 1975). Hyatt (1866) advocated changes in rates, acceleration and retardation, as the mechanism of evolutionary change. So we ®nd Cope citing Hyatt's approach: There is an increasing concentration of the adult characteristics in the young of higher species and a consequent displacement of other embryonic features which had themselves also previously belonged to the adult period of still lower forms. (Cope 1887, p. 809)

Hyatt developed the òld age' theory of species, in which species, like individuals, go through youth, maturity and old age before extinction. For Hyatt `the phenomena of individual life are parallel with those of its [the organism's] own phylum and both follow the same law of morphogenesis', while evolution is seen as `®rst taking effect as a rule upon the adult stage, and then through heredity upon the earliest stages in successive generations' (Hyatt 1893, pp. 374, 390±391). Such widespread in¯uence of Haeckel's biogenetic law prompted the following from the historian of biology Fred Churchill: We need to ask why it was that a whole generation of professionals, biologists of the rank of Weismann, Balfour, Lankester, and Hyatt, subscribed to and invoked the biogenetic law. Their diverse backgrounds and assertions belie that they all were seduced by the same idealistic philosophy as Haeckel. Even more to the point, how were their scienti®c achievements really possible if the ground beneath their castles consisted of the quicksand of recapitulation? (Churchill 1986, p. 12)

A further major in¯uence on palaeontology was exerted by Osborn, whose legacy was no less than the establishment of a single great school of vertebrate palaeontology based at Princeton and Columbia universities, and then at the American Museum of Natural History in New York, of which august institution Osborn was President for almost 30 years (Gregory 1938; Rainger 1991; Ruse 1996). Osborn obtained his embryological training from the English embryologist Francis Balfour, whose in¯uential school of evolutionary embryology at Cambridge attracted Osborn and a fellow Princeton undergraduate, W. B. Scott (Alexander 1969; Hall 2000a, in press a). In moving to palaeontology, Osborn deliberately abandoned embryology, claiming that he had no `talent in embryological techniques' (1930, p. 65). Nevertheless, the strongly biological basis of American palaeontology from the 1890s was due in large measure to Balfour's in¯uence on Osborn and on Scott (1917) although Scott later took a rather more cautious view of the evolutionary information to be found in embryos. Scott (1894) published a very critical review of Bateson's (1894) book Materials for the study of evolution, which was the ®rst great treatment of variation since On the origin of species. Like Bateson, Scott admitted the limitations of embryology and comparative anatomy as ®nal arbiters in the study of morphology. Scott also saw the consequences for palaeontology and palaeontologists if Bateson's central premise that individual variations form the material out of which new species are made. If Bateson was correct, then àll the paleontological phyla have been erroneously arranged and must be thoroughly reconstructed' (Scott 1894, p. 358). Scott outlined the fossil evidence demonstrating that variants, especially extreme variants, were not the basis for phylogenetic progress, remained a palaeontologist and stayed with the typological approach. The arrangement of the phyla remained until reordered by discoveries based on the Burgess Shale fauna and molecular biology (see below), while palaeontology went on to make signi®cant contributions to our understanding of the history of life. Some of those contributions are outlined below, with emphasis on those that had their basis in so-called `laws of construction', i.e. in the analysis of growth and development. CONTRIBUTIONS OF PALAEONTOLOGY

Deep time An obvious contribution of palaeontology is the provision of time (`deep time', Haber 1959) as a dimension to evolutionary change. As summarized eloquently in a history of vertebrate palaeontology in America: for him [the paleontologist] time means little in terms of his own life, and he can look into the past and see the great and fundamental changes which evolution has wrought, the rise of phyla, of classes, of orders, and he alone can see the orderliness of the process and sense the majesty of the laws which govern it. (Lull 1918, p. 246)


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The provision of a temporal dimension is not without its own problems when addressing the òrderliness of the process'; witness the controversy over the time of origin of animal `phyla' or animal `body plans', and whether there was a Cambrian èxplosion', as assessed by palaeoecological, molecular, palaeontological or developmental evidence (Brasier 1991; Valentine et al. 1991, 1999; Wray et al. 1996; Conway Morris 1997, 1998d, 2000a-c; Fortey et al. 1997; Hall 1998; Budd and Jensen 2000). Part of the controversy, and the reason for placing `phyla' and `body plans' in quotation marks, is that many systematists would see such groupings as having no value in phylogenetic analyses, individual character states being the only recognizable units. Not that characters are an infallible guide. Assessment of homology is critical for any method that compares two or more organisms or reconstructs phylogenies (Hall 1994). On the other hand, there has been much parallel evolution (homoplasy) throughout metazoan evolution (Sanderson and Hufford 1996). This is because characters can come and go while the molecular and developmental bases for those characters remains, and vice versa (Shubin 1998; Meyer 1999; Hall in press b), a ®nding that may turn out to be a key contribution of evo-devo to palaeontology and a caution when using cladistics to reconstruct phylogenies. Extinct life forms A second palaeontological contribution comes from the discovery of forms of organisms no longer extant, or the discovery of features no longer found in living forms; the `fascinating and poorly-understood exercise in complex pattern recognition [that] lies...at the heart of descriptive palaeontology' (Budd 2000, p. 12). Such discoveries, the Ediacaran fauna and dinosaurs are two obvious examples (Conway Morris 1998a; Cadbury 2000), have the potential to ®ll gaps in phylogenetic reconstruction, to establish homologies or identify convergence, and to document which morphologies are possible from what often seems an endless range of possibilities, continuing the trend of the evolutionary embryologists of the nineteenth century who pursued gaps in the fossil record using embryos as surrogate ancestors. In searching for the basis of the patterns seen in the fossil record, and as discussed in the next section, palaeontologists developed or adapted approaches based in laws of construction, i.e. in laws of development, morphogenesis and growth. Triangles, morphospace, constructional morphology Whether morphological diversity is open-ended or constrained, and how function can be inferred from the structures preserved in fossils, are two issues that palaeontologists have addressed, especially Martin Rudwick (the paradigm method), Adolf Seilacher (morphodynamics, Seilacher's triangle) and David Raup (morphospace). All three approaches contribute to and are applications and extensions of a tradition of constructional and functional morphology of extant organisms with considerable strengths in Europe (Dullemeijer 1974, 1991; Reif et al. 1985; Schmidt-Kittler and Vogel 1991; and the chapters in Splechtna and Hilgers 1989 as exemplars) and in North America (Raup and Michelson 1965; Raup 1966; Thomas 1979; Liem and Wake 1985; Gans 1988; Herring 1988; Liem 1991; Thomason 1997). Functional approaches also inform palaeontology (see below and the chapters in Thomason 1997) but as yet not to the same extent as constructional morphology. Rudwick (1964) developed a four-step paradigm method to infer function from fossil form: 1, characterize the structure; 2, specify a set of possible functions for that structure; 3, specify the ideal form for performing each function; and 4, compare the ideal and actual forms so as to ®t function with form, and identify optimality vs. trade-offs. The paradigm method has its limitations. It depends on analogies, assumes ideal morphology and performance, and, because it can be conducted outside of an evolutionary framework, does not necessarily indicate the origins of the features or functions. Now outmoded, it is perhaps best used to generate testable hypotheses rather than to provide de®nitive answers; for instance, it has been used by Hickman (1988, 1999) to analyze form and function in extant gastropods. Approaches based on phylogenetic inference (infer homologous features based on their distribution in related taxa) and extrapolatory modelling based

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upon form-function correlation and biomechanical design features, place such approaches on a ®rm phylogenetic footing (Bryant and Russell 1992; Witmer 1995). Conservation of (a) structure(s) across different functions provides prima facie evidence for a constraint on morphology and opens a window on the possible basis for that constraint. If one knew the possible morphologies for the range of designs an organism could exhibit, then designs found in nature could be plotted three-dimensionally in morphospace. The less morphospace occupied, the more limited the range of possible morphologies. Raup (1966) determined the morphospace occupied by extant and fossil gastropods, brachiopods, ammonites and pelecypods by plotting axes of shell growth. He found much of theoretical morphospace to be unoccupied by extant or fossil species; morphology is constrained and not all morphologies are possible. This method has wide applications in any phylogenetic analysis involving shape transformation (Raup and Stanley 1978; Hickman 1988) and can be tested against independent phylogenetic analyses. Seilacher (1970) resolved morphology into the three components of environment (ecological adaptation), architecture/fabrication (morphogenesis, structural laws) and phylogenetic legacy. Raup (1972) added chance and ecophenotypes as additional causal components, effectively turning Seilacher's triangle into a Raupian pentagon. A polygon emerged as Seilacher re®ned his categories, including developmental mechanics and developmental genetics within fabrication approaches based in theoretical morphology (Seilacher 1991). Seilacher (1979) tested his approach by its ability to predict a particular structure or range of structures from the range of possible structures among sand dollars. For her analysis of the morphological evolution of gastropod radulae, Hickman (1980) used seven factors: phylogenetic, mechanical, ecological, programmatic, maturational, degenerative and constructional. Perhaps the application of Seilacher's approach with the greatest impact is Gould and Lewontin's (1979) paper on constraint, BauplaÈne and organisms as integrated wholes, and Gould and Vrba's (1982) concept of exaptation, i.e. features that enhance ®tness now but that were constructed for a different role in the past. A subsequent major advance in the incorporation into palaeontology of even wider areas of biology than development, morphogenesis and growth was the rise of palaeobiology. PALAEOBIOLOGY

The study of the biological aspects of the history of life is palaeobiology. Many of today's palaeontologists are palaeobiologists. The term goes back at least to Abel (1912) and now embraces ecology, phylogenetics, community and population approaches, molecular biology, even behaviour, in quests to unravel the past. Over the last two decades textbooks on macroevolution and palaeontology have taken palaeobiology on board (e.g. Stanley 1979, 1981; Levinton 1988; Paul and Smith 1988; Allen and Briggs 1989; Eldredge 1995; Carroll 1997; Gee 1999; Briggs and Crowther 2001), and popular books on palaeobiology have appeared (Gould et al. 2001). The instructions for contributors to Paleobiology, `the purpose [of which] was at its inception in 1975, and remains, the uniting of paleontology with modern biology' (Sepkoski and Crane 1985, p. 1), indicate that the journal will consider (and that palaeobiology includes) studies on `macroevolution, extinction, diversi®cation, speciation, functional morphology, biogeography, phylogeny, paleoecology, molecular palaeontology, and taphonomy, among others' (Paleobiology 2000, 26, p. 165). Palaeontology is enriched and expanded by these approaches and so contributes new perspectives and insights to our understanding of the history of life (Conway Morris 1998a; Padian and RicqleÁs in press). In the preface to the 25th anniversary volume, Deep time: paleobiology's perspective, published by Paleobiology, Doug Erwin and Scott Wing (2000) listed the seven areas of palaeobiology addressed by the 15 papers in the volume. They include the properties of extinct organisms, chemical composition of fossils, the light fossils shed on genetics and development, how the palaeontological and stratigraphic record is to be interpreted, the in¯uence of environment on ecological systems and the evolution of lineages, the use of fossils to reconstruct phylogeny, and the role of fossils in understanding the processes that generate the large-scale patterns in the history of life. Many other disciplines interface with palaeontology (Table 1). Evo-devo is the latest.

TABLE

Field

1. Areas of overlap and integration between palaeontology and other biological disciplines Key references

Biomolecular palaeontology: the analysis of molecules preserved in the fossil record Runnegar 1986; Briggs et al. 2000 Palaeoanthropology, especially application of the concepts of neoteny and allometry Le Gros Clark 1955; Landau 1991; Shea 1993; Van Riper 1993; Lieberman 1997; Weiss and Buchanan 2000 Palaeoecology, palaeogeography, palaeobiogeography and palaeoclimatology1 Forbes 1846; Valentine 1973; Rehbock 1983; Berner 1993; Stanley 1995; Brenchley and Harper 1998; Conway Morris 1998a; Erwin and Wing 2000; and see the papers in the special insert Èarth's variable climatic past' in Science 2001, 292, 657±693 Palaeohistology Enlow and Brown 1956, 1957, 1958; Enlow 1969; Horner et al. 2000, 2001; RicqleÁs et al. 2000 Palaeoichnology: the analysis of trace fossils, trackways, footprints and impressions Gillette and Lockley 1989 Palaeopathology, palaeophysiology and forensic palaeontology Iscan and Kennedy 1989; Ortner 1993


Allometry, growth and heterochrony Gould 1977; Shea 1993; McNamara 1995; Hall 1999; Zelditch 2001

Taphonomy: the processes that determine the preservation of fossils Behrensmeyer and Hill, 1989; Allison and Briggs, 1991 1

Although these ®elds have undergone great recent transformations, they go back to Robert Hooke in the late seventeenth century, to Lyell and to Forbes.

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EVOLUTIONARY DEVELOPMENTAL BIOLOGY AND PALAEONTOLOGY

The goals and aims of evolutionary developmental biology are to understand: 1, the origin and evolution of embryonic development; 2, how modi®cations of development and developmental processes lead to the production of novel features; 3, the adaptive plasticity of development in life-history evolution; 4, how ecology affects development to modulate evolutionary change; and 5, the developmental bases of homoplasy and of homology. (Hall 2000b, p. 177, and see Robert et al. 2001) Several of these aims directly affect palaeontology, including: 1, how developmental constraints bias the direction of evolution (re¯ected, in part, in constructional morphology); 2, how micro-evolutionary developmental processes relate to macro-evolutionary differences; 3, the role of modules in development and evolution; 4, why there is a con¯ict between molecular clocks and the fossil record in timing the metazoan radiation; and 5, whether Precambrian metazoan ancestors were similar to larvae or to miniature adults. (Raff 2000) In the following, I consider some case studies of how approaches that integrated palaeontology and evodevo informed past research and hold great promise to generate an integrated life science for the twenty®rst century. Indeed, as the following section demonstrates, without evo-devo, the future contributions of palaeontology might well be stillborn and a far cry from the `science of the twenty-®rst century' (Conway Morris 1998a). Metazoan origins Conway Morris (1998b, c for summaries) has done much to establish our knowledge of the origins of animal phyla and the ecological conditions and ecosystems associated with that origin, especially as evidenced in the fauna of the Burgess Shale. Running ahead of the pack, as is his wont, Conway Morris wrote a forward-looking article on why molecular biology needs palaeontology, following it with analyses of how palaeontological and molecular data concerning early metazoan evolution could be reconciled, a perspective on the small number of molecular pathways involved, and the problems thereby raised for homology (Conway Morris 1994, 1998d, 2000a). Phylogenies obtained using the sequence analyses of rRNA revealed by molecular biology, required a signi®cant re-analysis of the phylogeny of the Metazoa incorporating molecular and palaeontological evidence. On the other hand, discoveries of shared genes such as homeobox genes demonstrated fundamental similarities underlying all animal body plans, suggesting that those genes underlie the origin of the similarities. How do such molecular and genetic studies impact on palaeontology? How is palaeontology to react? One attempt to reconcile the apparently contradictory evidence by invoking a palaeontological perspective to evo-devo, is a proposal by palaeontologist Graham Budd (1999) of `homeotic takeover', whereby adaptive modi®cations of structures come under the control of homeotic genes after the morphology arose, rather than homeotic genes having been required for the structure to arise; see Robert (2001) for a perspective on how we should interpret the role of homeotic genes in development and evolution. Even more fundamental is the nature of the relationship between the genotype and the phenotype. It is precisely because the phenotype is not a one-to-one read-out of the genotype that evo-devo exists. The need to open the `black box' of development has been recognized and manifested in various guises, essentially even since the cell theory was propounded. Those guises include (in a not exhaustive list): epigenesis vs. preformation; whether nucleus or cytoplasm `controls' development; genetic determinism; epigenetics; genetic assimilation; phenotypic plasticity; units of inheritance/heredity; phenogenetic drift; and developmental systems theory (Hall 1983, 1998, 2001; Weiss and Fullerton 2000; Robert et al. 2001; True and Hagg 2001; and the entries in Hall and Olsen in press). Understanding the origin and nature of


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body plans and phenotypes within the context of genotype-phenotype interactions will surely be a major achievement of any closer interaction between palaeontology and evo-devo. Body plans are all about similarity. Body plans remain and show a morphological continuity that is recorded in the fossil record. Conway Morris (1994, p. 9) listed ®ve aims of `mutual and reciprocal interest to palaeontologists and molecular biologists': 1, sample a great diversity of metazoans; 2, employ molecules other than rRNA in such analyses; 3, enhance our understanding of the biochemical pathways and physiological processes employed within metazoans; 4, discover how developmental mechanisms have evolved; and 5, understand the basis of the stability of body plans expressed within the Metazoa. Much progress has been made in these areas in the past seven years, in no small part because of the applications of phylogenetic analysis. The papers from four symposia organized by the Society for Integrative and Comparative Biology highlight much of this progress (Martindale and Swalla 1998; McHugh and Halanych 1998; Olsson and Hall 1999; Burian et al. 2000). For example, palaeontology speaks to the issue of where to draw the boundaries between groups of organisms. The absence of any fossil intermediates among phyla informs such fundamental concepts as `phyla' and `body plans', and forces us to consider how the absence of morphological intermediates matches with the ®nding that major developmental genes are conserved across all phyla, indeed across more than one kingdom. The enigmatic Ediacaran fauna and the early arthropods of the Burgess Shale have been used to marshal arguments against the view presented by Patterson (1981) that there may be no instance of fossil evidence overturning relationships between animals established using recent organisms or molecular data. In a fresh approach, Budd and Jensen (2000) challenged the twofold assumptions that all the `phyla' originated in the Cambrian èxplosion' and that, at their ®rst appearance, `phyla' were suf®ciently similar to crown groups in their characters that virtually all could be recognized as phyla. All fossils fall on a continuum between stem and crown groups (Smith 1994; Budd 1999; Budd and Jensen 2000). Indeed, assignment to a stem or a crown group must always be relative to a crown or stem group. There is no reason to expect organisms close to the origins of the major body plans to ®t into the designation `phylum,' a designation that we give to organisms which have evolved all the diagnostic characters of this major systematic category. Using phylogenetic approaches based on stem and crown groups to separate the origin of major groups from the origin of phylum-speci®c body plans, Budd and Jensen came to the conclusion that many phyla were not present in the earliest Cambrian. Although inescapable from their analysis, this conclusion may not sit well with much of the palaeontological community; indeed, it `will ruf¯e plenty of feathers' (Conway-Morris 2000b, p. 1056). Budd and Jensen considered such fundamental issues as the de®nition of phyla, whether metazoans arose as small bodied, larval-like organisms (they think not), and whether fundamental aspects of body plans such as the coelom arose once or more than once (they think once). From an analysis that epitomizes the challenges to entrenched thinking posed by combined phylogenetic, palaeobiological and evo-devo approaches to problems traditionally regarded as the preserve of palaeontology, the Cambrian èxplosion' emerges as an explosion of fossils, not an explosion of phyla or body plans; see Conway Morris (2000b, c). Such approaches bring a fresh vision to major questions concerning the patterns and processes of life. Fossil embryos An obvious example of a direct connection between palaeontology and evo-devo is the discovery of eggs, embryos, and larvae in the fossil record. The ®nds that have attracted the most attention are embryos of Neoproterozoic and early Cambrian metazoans (Zhang and Pratt 1994; Bengtson and Yue 1997; Xiao et al. 1998). Although they are enigmatic and open to interpretation (especially those from the Neoproterozoic), such ®nds are very signi®cant, both in their own right, and if they can be coupled with appropriate adults; they hold the potential to resolve theories of the origins of the metazoans that otherwise are based on analyses of embryos and larvae from extant organisms. Life cycles, including such fundamental features as the presence or absence of larvae,

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turn out to be surprisingly plastic (Hall and Wake 1999). Did metazoans arise from forms similar to present-day larvae or were early metazoans `direct-developers', larvae being (a) later addition(s) into the metazoan life cycle (Davidson et al. 1995; Peterson et al. 1997, 2000)? While palaeontologists will continue to search for evidence, at present no fossil evidence supports a larval stage in early metazoans, although larval stages of later (crown) groups are preserved (Conway Morris 1998d, e). Evo-devoists should take note of this evidence and incorporate it into their theories of metazoan origins. If we are fortunate, the fossil-rich strata in China will yield further fossil embryos. A suf®ciently large sample could inform analyses such as that by Valentine (1997), in which cleavage patterns in metazoan embryos could be ordered to support a pattern of evolution with only a single change from radial to spiral cleavage. They also will inform hypotheses of metazoan origins that provide robust phylogenies based on molecular evidence (e.g. Eernisse and Kluge 1993; Valentine et al. 1996, 1999; Wray et al. 1996; Collins 1998; Conway Morris 1998d, 2000a) or analyses that use `total evidence' from fossils, molecules and morphology (Eernisse and Kluge 1993, and see the papers in McHugh and Halanych 1998), although total evidence analysis is a controversial approach (Patterson 1981; Conway Morris 1994). Insights should also accrue from plotting sequences of derived developmental characters onto phylogenies that were generated using a set of characters other than the developmental characters being investigated. Middle ear ossicles A classic case where developmental, evolutionary and palaeontological approaches have informed our understanding of the origins and sequence of evolution of a feature, is the origin of mammalian middle ear ossicles in what were originally called the `mammal-like reptiles' (Kemp 1982). Changes occurred in the jaw joint and musculature, brain size, teeth, postcranial skeleton and diaphragm during this transition, in what is a text book case of mosaic evolution. The fossil record of the sequence of changes in the middle ear is augmented and fully supported by the development of middle ear ossicles in extant mammals, especially in marsupial embryos, in which the `reptilian' condition is replaced by the mammalian as embryonic development unfolds (Kemp 1982; Kermack and Kermack 1984; Hopson 1966; Rowe 1996; Carroll 1997; Smith and Nievelt 1997). The insights that arise from combining evo-devo with palaeontology are demonstrated beautifully in the recent analysis of Hadrocodium wui from the Lower Jurassic of China, the earliest known mammaliaform fossil and the nearest fossil relative of mammals. Luo et al. (2001) incorporated an in-depth analysis of the morphology of the fossils with data on the development and rates of development of the middle ear ossicles in extant marsupials and placentals, along with changing brain volume and middle ear ossicle development in Hadrocodium and more derived mammals. They showed the step-wise acquisition of mammalian characters, the likelihood that increasing brain volume played a role in the origin of the ear ossicles, and the diversity in body sizes and range of trophic diversity in these precursors of the mammals. Their analysis also demonstrates extensive homoplasy (both convergence and reversals), i.e. multiple origins, associated with the emergence of the mammals (see Wyss, 2001 on this point and Hall in press b for an assessment of homoplasy). An integrated `whole organism' view of the evolution of middle ear ossicles is emerging from such combined analyses. Fish ®ns to tetrapod limbs Another example of how palaeontology bene®ts evo-devo and vice versa is the transformation of ®ns to limbs in tetrapod evolution. New fossil ®ndings illuminate our understanding of limb development, even as developmental and molecular studies elucidate the fossil record of limb evolution (Coates 1991, 1994; Shubin 1995; Shubin et al. 1997, and see the papers in Olsson and Hall 1999). As one example, the ®nding by Coates and Clack (1990) that the earliest tetrapods such as Acanthostega had more than ®ve digits per appendage, i.e. were effectively polydactylous, overturned the entrenched view that tetrapod limbs were built on a pentadactyl plan, a view based on the presence of ®ve or fewer digits in the limbs of most crown-group tetrapods and on the developmental evidence of digit development (Hinchliffe 1994). Future fossil ®nds should clarify the nature of these digits for palaeontologists: are some


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digits bifurcations and/or duplications of existing elements rather than new elements; what is their relationship to the tarsals and carpals; what is the relationship of these digits to the radials in the ®ns of sarcopterygians? Such ®ndings will inform evo-devoists as they interpret patterns of Hox gene expression in ®n and limb buds that provide the basis for plausible scenarios of the molecular changes that accompanied the transition from ®n to limb (Duboule 1992; Duboule and Wilkins 1998). Limb loss in snakes The loss of limbs in snakes provides a further example of the advances that accrue when evo-devoists and palaeontologists address the same research problem. Insights have come both from the discovery of three fossil snakes with hind limbs, Pachyrhachis problematicus, Haasiophis terrasanctus and Podophis descouensi (Haas 1980; Caldwell and Lee 1997; Lee and Caldwell 1998; Coates and Ruta 2000; Greene and Cundall 2000; Tchernov et al. 2000; Wiens and Slingluff 2001), and from developmental and molecular analysis of limb bud development in extant snakes. The fossils demonstrate that hind-limb skeletal loss was progressive, with distal elements being lost ®rst, the three species lacking digits but retaining tibia, ®bula and femur. The positions of the limb buds in tetrapods is speci®ed via differential regulation of Hox genes, both in the lateral plate mesoderm, which is the precursor of the limb skeleton, and in the paraxial mesoderm, which provides the myogenic cells of the limb buds (Cohn et al. 1997; Burke 2000). Extant snakes lack fore limbs and fore-limb buds (Raynaud 1985). Changes in the expression boundaries of speci®c Hox genes in python embryos were interpreted by Cohn and Tickle (1999) as playing a leading role in the loss of the fore limbs; the anterior expression boundary has moved so far anterior that there is, in effect, no anterior expression boundary and so no signal to position the fore-limb buds. Some snakes develop hind-limb buds, even though, as adults, they lack hind limbs, the limb buds regressing early in embryonic life; some snakes, such as the python, do form rudimentary hind limb skeletal elements, consisting of a femur and terminal claw (Raynaud 1985). In limbed tetrapods, the anterior expression boundaries of HoxC-5 and HoxC-6 coincide with the where fore- and hind-limb buds develop. There is a Hox gene boundary in python embryos, and hind-limb buds are initiated, although they subsequently almost completely regress. Further developmental and molecular studies of the mechanisms of limb loss and limb skeletal rudimentation in snakes, combined with additional fossil ®nds, should enable us to more fully understanding the intriguing evolutionary transformation that is limb loss. Neural crest cells and craniate evolution The neural crest, neural crest cells and neural crest-derived skeletal and dental (odontogenic) tissues provide the ®nal example of a research programme that integrates evo-devo and palaeontology; see Langille and Hall (1989), Smith and Hall (1990, 1993), Smith et al. (1994), Graveson et al. (1997) and Hall (1998, 1999, 2000c, 2002) for more detailed information on this research strategy. The neural crest, a band of cells along the dorsal fold of the neural tube, was ®rst recognized in shark embryos in the 1800s (Hall 1999, 2000c). Neural crest cells arise from ectoderm at the boundary between neural and epidermal ectoderm. The suggestion was made in the early twentieth century that ectodermal neural crest cells produce mesenchyme, skeletal and dental tissues (Hall 1999). This was so foreign to the theory of the constancy of germ layers origins (the germ-layer theory) which dominated embryology and vertebrate palaeontology, that it was not until the 1980s that the neural crest origin of skeletal and dental tissues began to in¯uence our approach to embryology, evo-devo, and palaeontology (Smith and Hall 1990, 1993; Hall 1997, 1998, 1999). Interestingly, invertebrate palaeontology was much less in¯uenced by such biological strait-jackets as the germ-layer theory, having been àpproached so largely from the viewpoint of stratigraphic geology, that of the vertebrates [being] essentially a biologic science' (Lull 1918, p. 216). Three examples of studies involving neural crest cells are discussed. 1. An evo-devo approach to the evolutionary origins of the neural crest informs craniate origins. The neural crest is a vertebrate (craniate) synapomorphy not found in cephalochordates, such as amphioxus,

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protochordates or urochordates, and so must have arisen with or near the origin of the craniates. A search among non-vertebrate chordates reveals few morphological clues of a `protoneural crest' in either epidermal or neural cells. However, recent studies on the expression in Branchiostoma (amphioxus) and in ascidians of genes that are found in the neural crest in craniates, provide some tantalizing clues of what the neural crest precursor may have been (Holland 1998, and see Hall 1999, 2000c, and the papers in Olsson and Hall 1999, especially Holland and Holland 1999). Assessment of such ®ndings against descriptions of Early Cambrian cephalochordates or hemichordates (Yunnanozoon, Cathaymyrus; Chen et al. 1995; Shu et al. 1996a, b) promises to be a productive research programme, with study of the neural crest revealing cellular origins and mechanisms, and the fossils revealing the earliest neural crest derivatives. 2. The existence of novel neural crest-derived skeletal tissues provides an opportunity to open a developmental window onto how skeletal tissues arose. Secondary cartilage is such a tissue. Secondary cartilage, which arises on dermal membrane bones, is con®ned to birds and mammals and (so far?) to one species of teleost ®sh (Smith and Hall 1990, pp. 330±332; Hall 2000c). Extant reptiles lack secondary cartilages. When did birds acquire secondary cartilage? Given the overwhelming palaeontological evidence for the origin of birds from theropod dinosaurs (Carroll 1997), the distribution of secondary cartilages in extant vertebrates indicates that theropods among fossil forms, and crocodilians, turtles and other extant archosaurs, should be examined more thoroughly for the presence of secondary cartilage than they have been in the past. Discovery of embryonic theropod skulls, with the state of preservation of those of sauropod dinosaurs (Chiappe et al. 2001), coupled with palaeohistology, would give us the palaeontological information on presence or absence of secondary cartilage. Developmental studies should target whether the secondary cartilages of birds and mammals are homologous (Hall 2000c). 3. Evidence from embryological mechanisms operating in contemporary vertebrates is the basis of arguments for the parsimony and conservation of embryological mechanisms throughout vertebrate evolution, a nice parallel to the uniformitarianism of geology. Consequently, by using knowledge of features that arise in neural-crest cells in extant vertebrates, embryological experiments can be devised to shed light on the origin of the same or related features in extinct vertebrates. As summarized by Maisey (1986, p. 242), the history of the skeletal system in vertebrates can best be understood through the `reciprocal illumination' that comes through a combined palaeontological and developmental biological approach, an approach pioneered for skeletal tissues by Schaeffer (1977) and Schaeffer and Thomson (1980). Palaeontologists such as Robert Carroll and his students incorporate a developmental perspective into their studies of the origin of amphibians, amphibian vertebrae, patterns of limb ossi®cation, and adaptations in skeletal development in mososaurs and ichthyosaurs. They inform their palaeontological analyses with information on homology, resegmentation of somitic mesoderm, patterns of vertebral and limb ossi®cation, and altered timing of skeletal development derived from embryos of extant species (Carroll 1989, 1997; Caldwell 1994, 1997a, b; Carroll and Chorn 1995; Carroll et al. 1999). [Heterochrony (Table 1), change in timing of development in a descendant in relation to timing in an ancestor, has, of course played an important role in palaeontology. Unfortunately, space does not allow heterochrony to be treated (see the references in Table 1)]. Carroll's latest book, Patterns and processes of vertebrate evolution (1997), is an outstanding example of the insights that come when a palaeontologist takes on board an evo-devo perspective, integrating palaeontology, development, developmental mechanisms, and developmental and quantitative genetics. Another prominent palaeontologist regarded the book as: the most important book in vertebrate evolution since Simpson's Tempo and Mode in Evolution (1944) because of what it offers as a summary, an integration, and above all a prospectus for vertebrate biologists of a new synthesis that is showing all signs of a very healthy infancy. (Padian 1997, p. 1083)

A major advantage of skeletal and dental tissues for analyses combining developmental and palaeontological approaches is the remarkable degree to which these tissues are preserved in the fossil record, combined with the fact that tissues that are hundreds of millions of years old can be recognized and categorized on the basis of our knowledge of tissues in modern vertebrates. Smith and Hall (1990) provided a review of such an approach with reference to the development and evolution of skeletal and dental tissues, forging a synthesis of knowledge derived from extant and fossil taxa that includes a


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classi®cation of these tissues in both the exo- and endoskeletons (ibid., Table 1, pp. 317±318) as well as 12 postulates concerning the origin of these tissues (ibid. pp. 349±352). Smith and Hall (1993) undertook a conceptually similar analysis of the relative contributions of cranial and trunk neural crest to the origin of skeletal and dental tissues. Speci®cally, Smith and Hall examined the neural crest-derived dermal (exo-) skeleton, which in some early agnathans formed an armour that could extend from snout to tail. The tissues that comprised this armour were dentine (now regarded as primarily a tissue of teeth) and bone. Such an extensive dermal armour would most plausibly have arisen from trunk neural crest cells (i.e. cells that migrate out of the developing spinal cord) rather than from cranial neural crest cells (cells that migrate out of the developing brain), although the dermal skeleton in all extant vertebrates (or, at least in those studies; the data base is con®ned to a few species) arises from cranial crest cells; trunk crest cells form neither skeletal tissues nor teeth (Smith and Hall 1993; Hall 1999, 2000c). Using an approach involving recombination of trunk neural crest cells with cranial epithelia known to evoke tooth and skeletal development, Lumsden (1984, 1987) and Graveson et al. (1997) demonstrated that the most cranial (rostral) trunk neural crest of mice and urodeles can form teeth. Assuming conservation of developmental mechanisms, although development can, of course, evolve (Raff 1996; Hall 1998; Wagner et al. 2000), these experiments allow us to interpret the extensive dermal armour of fossil forms as having originated from trunk neural crest, cause us to re-evaluate the `dichotomy' between a skeletogenic and odontogenic cranial crest and non-skeletogenic and non-odontogenic trunk crest, and indicate that separation of cell lineages producing craniate endo- and exoskeletons occurred over 500 million years ago. Evo-devo sheds light on palaeontology in experiments that could not have been undertaken in the absence of the palaeontological data on dermal armour. CONCLUSION

These are some of the reasons why palaeontology needs evo-devo and evo-devo needs palaeontology. Links to evo-devo are the latest manifestation of long and deep connections between palaeontology, embryology and evolution. Indeed, it can be argued that palaeontology cannot effectively contribute to evolution without incorporating evo-devo. The conceptual advances and understanding that come from such combined or integrated studies will transform palaeontology into a science of the twenty-®rst century and holds every prospect of illuminating, perhaps even changing fundamentally, our understanding of the origin, maintenance and evolution of life. Evo-devo also gains from the ability to map developmental changes onto the fossil record and to design experiments based upon questions generated by the fossil record. Acknowledgments. I thank Graham Budd, Simon Conway Morris, Tim Fedak, Wendy Olson, Kevin Padian, Jason Robert, Jon Stone, and Matt Vickaryous for their critical comments on the manuscript. It was a very different paper before they attacked it. My thanks also to the participants in Biology 4811/5811, whose lively discussion of the paper also lead to improvements. My apologies to those in the various ®elds discussed whose work could not be cited because of limitations of space. Support in aid from the Natural Sciences and Engineering Research Council (NSERC) of Canada and from the Killam Trust of Dalhousie University is gratefully acknowledged. REFERENCES È ge der Palaeobiologie der Wirbeltiere. Verlag Schweizerbart, Stuttgart, 708 pp. ABEL, O. 1912. Grundzu AGASSIZ, A. 1850. On the differences between progressive, embryonic, and prophetic types in the succession

of organized beings through the whole range of geological times. New Philosophical Journal, Edinburgh, 49, 160± 165. ALEXANDER, T. E. 1969. Francis Maitland Balfour's contributions to embryology. Unpublished PhD Thesis, The University of California, Los Angeles, CA, 182 pp. ALLEN, K. C. and BRIGGS, D. E. G. 1989. Evolution and the fossil record. Smithsonian Institution Press, Washington, DC, 265 pp. ALLISON, P. A. and BRIGGS, D. E. G. 1991. Taphonomy. Releasing the data locked in the fossil record. Plenum Press, New York, 560 pp.

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Department of Biology Dalhousie University Halifax, Nova Scotia Canada B3H 4J1 e-mail [email protected].