Telomes, theory change, and the evolution of vascular plants

Review of Palaeobotany and Palynology, 50 (1987): 115 126 Elsevier Science Publishers B.V., Amsterdam Printed in The Netherlands

115

TELOMES, THEORY CHANGE, AND THE EVOLUTION OF VASCULAR PLANTS B E N T O N M. STIDD Department of Biological Sciences, Western Illinois University, Macomb, IL 61455 (U.S.A.)

(Received April 4, 1986; revised and accepted August 19, 1986)

Abstract Stidd, B.M., 1986. Telomes, theory change, and the evolution of vascular plants. Rev. Palaeobot. Palynol., 50:115 126. Evolutionary theory has been dominated by the so-called "modern synthesis" since its inception in the 1930's. Zimmermann's telome theory incorporates the same gradualistic assumptions as the modern synthesis and has nurtured and molded thought patterns of paleobotanists and students of plant evolution. Telome theory, like the modern synthesis, should not be faulted for what it includes so much as for what it excludes. Telome theory emphasizes evolution by terminal additions to successive ontogenies but is usually employed descriptively as if mature organs have undergone webbing, fusion, recurvation and the like. Thought patterns of this sort are necessarily gradualistic and do not recognize internal factors controlling development that might affect non-terminal stages. Interpretation of vascular plant phylogeny has been overly constrained by assumptions and mechanisms that occupy the core of the modern synthesis. Certain nongradualistic explanations for the evolution of selected organisms are reviewed and attention focused on the role of internal constraints controlling ontogenetic pathways and their macroevolutionary consequences.

Introduction P a l e o b o t a n i c a l views on the e v o l u t i o n of v a s c u l a r plants h a v e been d o m i n a t e d by a few f u n d a m e n t a l c o n c e p t s and c e r t a i n modes of t h o u g h t . F o r e m o s t a m o n g these in the 20th c e n t u r y has been the telome t h e o r y as formulated by Z i m m e r m a n n (1930) in G e r m a n y and as applied by S t e w a r t (1983) in N o r t h America, in his r e c e n t text. I will a t t e m p t to assess the v a l u e of the telome t h e o r y (and o t h e r related concepts) in e x p l a i n i n g the e v o l u t i o n of vascular plants as well as its place in the s t r e a m of e v o l u t i o n a r y t h o u g h t as it has developed in this c e n t u r y . I will c o n c l u d e t h a t while the telome t h e o r y and its u n d e r l y i n g g r a d u a l i s t i c a s s u m p t i o n s h a v e been i m p o r t a n t in s h a p i n g our c o n c e p t s of v a s c u l a r p l a n t evolution, 0034-6667/87/$03.50

f u t u r e a t t e m p t s to u n r a v e l the p h y l o g e n y of v a s c u l a r plants could profit from g r e a t e r attention to d e v e l o p m e n t a l p h e n o m e n a i l l u m i n a t e d by r e c e n t a d v a n c e s in o u r u n d e r s t a n d i n g of genome structure. T e l o m e theory F o l l o w i n g the d i s c o v e r y of the R h y n i e C h e r t plants and t h e i r p r o f o u n d influence on morphologists, Z i m m e r m a n n (1930) f o r m u l a t e d his telome t h e o r y as a basis for the ~new morphology". While it is g e n e r a l l y a c k n o w l e d g e d t h a t its utility is r e s t r i c t e d for the most p a r t to simple (primitive) Paleozoic plants it has n e v e r t h e l e s s provided a w a y of t h i n k i n g a b o u t p l a n t e v o l u t i o n t h a t t r a n s c e n d s its acknowledged domain. It is s o m e w h a t p a r a d o x i c a l t h a t

((: 1987 Elsevier Science Publishers B.V.

116

the telome theory should have come out of Germany and taken root in America. Germany was the fatherland of Goethe and the essentialism that undergirded Naturphilosophie. During the time the modern synthesis was being forged, German paleontology was dominated by Schindewolf's typostrophism, known in this country for its emphasis on orthogenesis and saltation (see Reif, 1983, for a good account of these matters). Nevertheless, as early as 1943 Germany produced a series of volumes edited by Heberer (1943) that was similar in outlook to that of the emerging modern synthesis. The Heberer (1943) volume included an article by Zimmermann, who was one of the evolutionists in Germany whose thinking was in tune with the shapers of the modern synthesis in North America. Perhaps the most notable difference in the development of 20th century evolutionary thought between Germany and the U.S.A. concerned the contribution of paleontology, as exemplified by Schindewolf (1936, 1950) and Simpson (1944), respectively. Zimmermann's views on evolutionary modes were much more closely aligned with Simpson than with Schindewolf. According to telome theory the evolution of vascular plants is a matter of gradual transformation as telomes undergo the familiar morphogenetic processes of planation, recurvation, fusion and webbing. Underlying these phenotypic changes are corresponding changes in the genetic messages that control development. The transformation of the vascular-plant body as various organs were fabricated out of telomes was accomplished, for the most part, by mutations affecting terminal stages in the developmental process (ontogeny). All the familiar evolutionary mechanisms elaborated by the modern synthesis - adaptation, selection, accumulation of small changes - - are efficacious, over time, in transforming simple telomic Rhynia-type plants into their more complex descendants. Paleobotanical research has been motivated by the expectation of finding enough of the fossilized intermediates resulting from this process to piece together phylogenetic history.

Although it is often de-emphasized and/or otherwise lost in descriptive accounts of how telomes produced various portions of vascularplant bodies, Zimmermann did tie his phylogenetic theories to ontogeny. He explicitly referred to this connection as "hologeny" and created an ascending spiral diagram that depicted the course of evolution as a series of ontogenies (see fig.9.11 in Stewart, 1983, and fig.3-15 in Foster and Gifford, 1974, and accompanying discussion). I am not overly perplexed when Stewart, for example, provides an account of how this or that organ or taxon evolved in terms of positional shifts C~phyletic slide") of mature structures in relation to one another (sporangial position in relation to sterile appendages in lycopods and sphenopsids). It is clear enough that Stewart perceives evolution as proceeding by modified ontogenies mediated by changes in embryos and meristems as surely as did Zimmermann. The point to be made here is that even though workers were aware of the necessity for evolutionary change to be accomplished by modified ontogenies, gradualism so dominated thinking that developmental factors influencing the course of evolution were made to fit with the common gradualistic conception of how evolution proceeds. This is not all bad. There are many features of vascular plants that have evolved gradually; the progressive enclosing of megasporangia by telomic units is an often cited example. In the late Silurian/early Devonian simple Cooksonia/Rhynia-type plants, having relatively recently emerged onto land or at least having recently acquired terrestrial land plant features (vascular tissue embedded in cylindrical parenchymatous axes, cuticle, stomata, etc.), had little chance of producing radically new structures in rapid order. By way of contrast the mid to late Cretaceous ancestral angiosperms possessed a degree of morphological complexity potentially capable of rapid production of new structures and new morphologies. Consider a Cooksonia apical meristem and apical meristems of mid-Cretaceous angiosperms, Sapindopsis for example. The genome

117

in the cells of the early angiosperm was the product of a long history of morphological innovations inherited from pteridophytic and gymnospermic ancestors. No doubt much of the ancestral genomic information was present (but unexpressed or so highly altered as to be difficult to express) in the cells of the early angiosperm meristems (embryo or shoot apex). Such a genome is a highly regulated conglomeration of bits of information. Just how this information is translated into its corresponding phenotype is still largely a black box. However, we know enough about what must transpire in this developmental black box to make the present analysis plausible. My point is simple. It is much more likely that new morphological features will be produced in short periods of time from a complex genome (our early angiosperm) than from a much simpler genome such as was the case in early Devonian plants; not inevitable, but more likely. The early Devonian genome also had a history - - a genome inherited from algal and perhaps bryophytic-type ancestors. I think it is unlikely that the bits of information coding for algal features would have had survival value if shuffling of the Devonian regulatory system had mananged to call them forth. New features with survival value would most likely be modifications of existing ontogenetic pathways or terminal additions. The latter particularly would involve considerable time to accumulate the necessary mutations. This process is what telome theory assumes and would result in a series of intermediate forms connecting later more highly evolved taxa. As recently as 1976 Doyle and Hickey, following Beck, could say without fear of contradiction that "... the concept of saltational evolution is unacceptable in the light of modern knowledge of developmental genetics" (Doyle and Hickey, 1976, p.184). Yet they suggest later in the same paper with regard to their hypothesis of angiosperm leaf evolution that "... some kind of fundamental reorganization of ontogenetic patterns and mature form ..." must have been involved. This reorga-

nization was accomplished in their scenario however in typical modern synthesis fashion [even in the "hardened" version (Gould, 1983) that ruled out inadaptive phases in founding new types] in that the reorganization occurred as the result of the ancestral seed fern tracking a xerophytic bottleneck. Upon resumption of mesophytic conditions, leaf expansion was accomplished in a new way, i.e. by intercalary growth. The trend toward more highly ordered venation patterns observed in the Potomac sequence represents successive modifications of developmental processes controlling the production of tertiary and higher vein orders. As is so often the case it is the initial stages in the transition from one type to another that are missing. Doyle and Hickey (1976) give a very plausible account of how this transition might have been accomplished. This is good science; an explanation is offered that is in line with the prevailing theory. The pattern observed (abrupt origin of a reticulate venation, albeit poorly organized, followed by a long period of refinement) did not bring the prevailing theory into question. Rather, the pattern was made to fit the theory. One purpose of this paper is to suggest that saltational evolution should be given a reconsideration. This is not to suggest that a hopeful monster should be expected at every branching point; its frequency is not proportional to its importance. Possessing the wisdom to discern where gradualistic evolution as exemplified by the telome theory does and does not apply is an ever present challenge. The p o s t - t e l o m e era

Evolutionary theory is in a state of ferment. The modern synthesis is undergoing attack on several fronts; old concepts are faltering and new concepts are emerging. There is a general awareness that developmental factors (ontogeny) played a very minor role in the modern synthesis and that the time is right to correct this deficiency (Bonner, 1981; Brooks and Wiley, 1986, p.3). Darwin knew nothing of the mechanism of inheritance nor what controls

118 development; thus the mechanisms he proposed to account for the sequence of forms entombed in the earth's crust were of necessity extrinsic - - environmental forces imposed on organisms (O'Grady, 1984). This orientation carried right through the modern synthesis and is only now losing its all-sufficient explanatory power. Developmental factors that control the ontogeny of organisms are necessarily intrinsic, and given the reasonably hospitable environment on this planet, many new phenotypes arising out of perturbations of ontogenetic systems are able to impose themselves on the environment. It is ironic that this latest addition to the synthesis threatens to displace selection (of small effect mutations over time) as the driving force of evolution. How does all this bear on our discipline (paleobotany) and on our understanding of the evolution of vascular plants? How do new morphologies arise, morphologies that we grace with various taxonomic designations? The following quote from Doyle and Hickey (1976, p.183), expresses the standard view. One of the most important tasks of the modern synthetic theory of evolution is to explain the macroevolutionary changes from one major adaptive type to another (usually equivalent to the origin of higher taxa) in terms of the same process of selection and accumulation of random minor mutations that are believed to be responsible for microevolutionarychanges at and below the species level. One of the tasks of paleobotanists is to document the chronological sequence of plant forms (taxa) in time and space. The typical paleobotanical paper describing some newly discovered taxon characterized by distinct morphological features will offer some passing comments on how the new form might have evolved. More synthetic works (review articles, textbooks) provide more sweeping explanations for the evolutionary pathways described. Commonly authors are content to outline phylogenetic pathways or as often as not merely to describe and summarize the various taxa; the explanations of the perceived pattern(s) are embedded in a host of underlying principles and assumptions about evolutionary

mechanisms. Rarely, almost never, has the perceived pattern led students of morphology/systematics to question the sufficiency of the mechanisms recognized by standard evolutionary theory. More than a decade after our paleozoological counterparts (Eldredge and Gould, 1972) questioned the sufficiency of standard evolutionary theory (phyletic gradualism), paleobotanists, some in this symposium volume, are beginning to invoke non. gradualistic explanations for the origin of key innovations in the evolution of vascular plants. [See Stidd (1985, p.107) for a brief discussion of the relationship between punctuated equilibria and neontological theories of change.] The remainder of this paper is devoted to an exploration of possible developmental mechanisms that may have punctuated the long history of vascular plant evolution. Morphology as a primary datum If a paleobotanist were to encounter two fossil plants as morphologically distinct as corn (Zea mays) and teosinte, its presumed immediate ancestor, there is little doubt that the two species would be placed in widely divergent taxa. This would be particularly true if only the female inflorescences were known and found isolated and unattached, as is usually the case, i.e. if the nature of the other plant organs were unknown. There the matter would lie until some of the dispersed and unknown parts were pieced back together. Even if the two species were entirely restored it would still come as a shock to learn that the two morphologically distinct forms were nearly identical genetically. Nevertheless we know this to be the case for the present example (Iltis, 1983, Walbot, 1983; Doebley et al., 1984). A notable instance of a similar situation in the animal kingdom is t h e relationship between humans and chimpanzees. These two species with their distinct morphological and mental differences are nevertheless nearly identical at the biochemical level (King and Wilson, 1975). Genome analysis at the chromosomal level (Yunis and Prakash, 1982)

119

has established t h a t the major visible differences are one fusion, six inversions and position of nuclear organizers. This pattern of large morphological differences and certain visible chromosomal differences together with small biochemical differences has focused attention on regulatory genes, rather than structural genes, as a possible explanation for presumed evolutionary pathways without finely graded series of intermediates. This is not to imply that regulating genes can carry the entire explanatory burden in these instances; indeed a typical modern synthesis explanation is still preferred by many as an adequate explanatory basis for the relationship between maize/teosinte and man/chimpanzee (Charlesworth et al., 1982; Coyne and Lande, 1985). Nevertheless several lines of evidence from paleontology (pattern assessment), molecular genetics and, most recently, morphogenesis/development, together with a new willingness to examine philosophical assumptions have caused a growing number of workers to invoke new explanations for morphological patterns they perceive in space and time. In the corn/teosinte and human/chimp examples, where phylogenetic relationships are reasonably clear and biochemical similarities have been established, morphology turns out to be a good criterion of critical changes in genomic or developmental factors controlling the phenotype. In this sense morphology (pattern) is a primary datum with which other data (process) must be reconciled and not the other way around as Ayala would have it "... any theory of macroevolution that is correct must be compatible with the theory of population genetics ..." (Ayala, 1983, p.284).

Canalization and recanalization Do sphenopsids have whorled appendages and sporangiophores because these features somehow conveyed an advantage that led to their fixation in a progenitor population? Does Rhynia major lack typical vascular tissue (xylem) while its smaller neighbor Rhynia gwynne-vaughanii (which presumably would

have less need for efficient water conduction) nevertheless possesses typical xylem because natural selection favored two different conduction systems in morphologically similar plants growing in the same bog? Are stigmarian roots spirally arranged and have abscission zones at their base because the genes that control this feature were selected for in some ancestral population? How many examples of this kind are necessary to cause one to question the sufficiency of accumulation of genes-of-smalleffect- over- time- po wered- by- natural- s election explanation which is at the core of the modern synthesis. Stigmaria is a good example of canalized structure that is not easily altered; abscission zones at the base of spirally arranged appendages are characteristic of leaves, not roots. Apparently the genome in this and related taxa was so constrained that shoot characteristics were retained in organs taking up existence underground, or shoot characteristics were expressed in organs that had become geotropic. But constraints are sometimes broken and new and different morphologies emerge. Students of plant morphogenesis felt little need to look for mechanisms that would account for abrupt morphological change so long as paleobotanists assured them that such changes were not necessary and so long as morphological gaps in the fossil and extant record were regarded as informational or preservational gaps. The monumental discoveries in this century, first of mendelian genetics and then its application to populations, were so captivating and so well grounded in observation and experiment that it was very natural to expand this knowledge into an all sufficient explanation for the evolution of organisms. These achievements were so well founded and so dominated thought patterns as to cause paleontologists, led by G.G. Simpson, to make the morphological and taxonomic patterns they observed conform to the mechanisms so successfully established by their neontological colleagues. Thus the modern synthesis was forged. It could hardly have been otherwise. Yet the "gradualistic and

120

adaptationist" glue that held the modern synthesis together has come under increasingly stronger scrutiny in the last decade. As selection and accumulation of small-effect mutations diminished as a satisfactory explanation, attention has shifted to genetic and epigenetic factors as internal generators of form (Alberch, 1982; Goodwin, 1984). Abandonment of gradually shifting morphology and emphasis of morphological stasis over time under punctuated equilibrium has reoriented thought patterns about the evolutionary process. Genome and/or developmental stability has become an attractive alternative to stabilizing selection as an explanation of stasis. Morphological stasis becomes a genomic/ developmental rather than a selection phenomenon and one looks for internal rather than external (environmental) forces to account for transitions between stable morphologies (Ho and Saunders, 1979). These transitions are highly constrained by internal structure of the genomic/developmental systern and impose a deterministic component on the speciation process and the course of evolution; taxa in morphospace are therefore clumped rather than evenly distributed (AIberch, 1982). But there is a lot of room for variation within genomic/developmental systems. Waddington's (1975, p.259) epigenetic landscape (a system of bifurcating channels and ridges on a tilted plane through which "development" rolls) can tolerate a lot of nucleotide substitution, transpositions and other genomic alterations without substantially altering the development system and the consequent phenotype. But on occasion, as in sickle-cell anemia, a small change at a critical place in genome structure may cause a large change in the phenotype. A species genome is analogous to large macromolecules (hemoglobin for example), that may undergo amino acid substitutions rather freely in noncritical areas but much less freely at functional interactive sites. Changes at sites that are involved in complexing with other molecules may on rare occasions lead to new functional breakthroughs;

similarly for genomes. Chromosomal aberations of transposed elements may on occasion lead to changes in the regulatory system that reverberate throughout the normal pattern of development, ultimately resulting in a new and stable genomic "configuration"; speciation is often achieved in the process. [But see Arthur (1984, p.178) who accepts saltational changes at the megaevolutionary level (classes and phyla) while downplaying their importance at speciation. He distinguishes his position from punctuated equilibrium on this basis. See also Oster and Alberch (1982) on the variable relationship between speciation and the origin of new morphologies.] If, according to the punctuational view, species are stable through time ( + 9 5 % of their existence) and if this stability is due to internal genomic as opposed to external (environmental) constraints, then we have a fundamentally different view of the evolutionary process. Under this view variability in populations cannot automatically be assumed to provide the basis for phylogenetically significant change; it may merely be "evolutionary noise" irrelevant to the generation of macroevolutionary patterns. If this view proves to be even partially correct, students of population dynamics must ask what stage in the history of a species their samples represent. What emerges as significant for future investigation is the stability of genetic systems (as judged by significant phenotypic changes) not the trivial change (from the macroevolutionary perspective) that allows a species to fine tune itself to the contingencies of the immediate environment. Kauffman (1983) has done some very interesting theoretical work which suggests that simple genomes with four kinds of genes (cisacting, trans-acting, structural and empty) and simple permutations of possible ways of interacting result in similar regulatory networks and similar genomic architectures. Such computer simulations demonstrate how genomes might become self-regulated in the absence of external, environmental selection with a view toward assessing how strong selection would have to be to overcome self-generated self-

121 regulating networks. ~'The quite surprising result of these studies is that such randomized genetic networks, rather than exhibiting uselessly disordered behavior, spontaneously exhibit extraordinarily constrained, ordered dynamical properties, reminescent in many respects to those found in contemporary cells" (Kauffman, 1983, p.217). Furthermore '~... 60 70% of the genes settle into fixed 'on' or fixed 'off' states", which constitutes a large block of considerable inertia that effectively isolates smaller gene clusters. These functionally isolated clusters exhibit oscillatory patterns of gene activity that constrain or channel the entire genetic system into certain patterns controlled by the possible combinations of products of the functionally isolated subsystems. We have then a regulatory network that can evolve piecemeal because mutation in one semi-isolated subsystem may alter the product of the total system without upsetting the products of the subsystems. Kauffman goes on to suggest how such a system might result in directed or oriented changes in developmental pathways that we might read from a macroevolutionary perspective as orthogenesis. A most fascinating possibility to emerge out of such a system is the re-expression of former structures such as teeth in birds (Kollar and Fischer, 1980) or, if I might be so bold, Psaronius features in Angiopteris or other extant marattialian genomes. In spite of the tremendous expansion of our knowledge of the vascular plant fossil record in the last several decades, relatively little progress has been made in understanding transitions between major taxa; higher taxa continue to be connected with dotted lines indicating uncertainty. No doubt future discoveries of new architectural forms will provide new understanding of transitions between major groups; we should continue to search. But at the same time we should be alert to canalized mental pathways that dominate the interpretation (or lack of interpretation) we make of new discoveries. It is an underlying assumption of this paper t h a t the dotted lines connecting major groups are precisely where

the modern synthesis and telome theory are most inadequate as explanatory theories. I suspect also that the extent to which readers will find this paper of value in solving these long-standing problems is rather directly correlated with the extent to which one is dissatisfied with standard evolutionary theory. The thrust of this paper is to suggest that transitions between major groups and architectural forms need be neither slow nor gradual.

Prospectus Contemporary paleobotanists have access to a growing body of literature by neontologists who are exploring non-gradualistic evolutionary mechanisms. Hilu (1983) discusses the role of large magnitude mutations in accomplishing transspecific evolution in flowering plants. "The various mutations cited here represent evolutionary trends that contributed to the initiation of new higher categories in flowering plants. The mutations show that the taxonomically important changes could have arisen abruptly" (Hilu, 1983, p.121). Gottlieb (1984) in a slightly more conservative report surveyed the literature on the genetics of morphological characters of flowering plants, stimulated by current controversy about macroevolution. He concludes that while characters such as differences in dimension, weight and number may be largely continuous and polygenic, other characters such as structure, shape, orientation and presence/absence are often discontinuous and governed by one or two genes. He attributes these discrete character differences to "...a direct consequence of the open, less integrative, and plastic patterns of plant morphogenesis which permit large changes in morphology on the basis of relatively few genetic changes" (Gottlieb, 1984, p.704). Bachmann (1983) also challenged the assumption that complex morphological characters have a complex genetic basis and its corollary that evolutionary distance is proportional to morphological distance. These assumptions were central to the synthetic theory

122 which emphasized the polygenic basis of morphological characters and believed evolutionary (morphologic) change to be a matter of changing allelic frequencies in populations. Though mutations with large morphological effects were known, evolutionists of the time were wary of a revival of mutationism (spearheaded by Goldschmidt), and large-effect mutations were dismissed as being too rare to be important. Bachmann (1983) recounts the interesting case of Crepis (Compositae) where a few plants in one species were discovered with well developed paleae (modified leaves subtending the flowers in flowering heads), structures which had been considered vestigial or at least in the process of being lost. The assumption that such structures are polygenically controlled (and therefore unlikely to re-evolve after being lost) was shaken by the demonstration that their presence or absence was determined by two alleles of a single mendelian factor. "Obviously there are higher order regulating genes that can suppress or activate the development of entire organs" (Bachmann, 1983, p.159). He cautioned against attributing too much to the direct action of regulatory genes, however, and argued for the efficacy of epigenetic processes t h a t allow for chance interaction of gene products and consequent emergent morphologies. An example of interest to paleobotanists is his account (Bachmann, 1983, p.172) of the factors involved in the handedness of spiral phyllotaxies - - a matter of the random positioning of the third leaf primordium in a seedling and the resulting clockwise or counterclockwise spiral. Also of interest is his account of how one of a member of heteroblastic organs may come to predominate. "What may primitively be a direct physiological (epigenetic) response to an environmental factor may become connected with a genetically triggered response to a symbolic environmental signal." This is similar if not identical to Waddington's (1975, p.59) concept of genetic assimilation. Easily the most striking example of rapid origin of a taxon in contemporary literature however, is the Catastrophic Sexual Transmu-

tation Theory (CSTT) for the origin of corn

(maize)=Zea mays ssp. mays) (Iltis, 1983). According to this view corn originated from wild teosinte (Zea mays mexicana or parviglumis) by the sexual conversion of the teosinte male inflorescence (tassel) into the female lateral inflorescence of corn. Archeological evidence indicates that domestication occurred about 7500 years ago. Teosinte and maize ears are so strikingly dissimilar morphologically that the two species were placed in separate genera for over 100 years. Yet the two taxa have the same chromosome number and structure (Kato Y, 1984) and are very similar at the biochemical level (Doebley et al., 1984). Iltis rejects the rather elaborate pathways by which the teosinte ear may have evolved into the maize ear postulated and diagrammed by Galinat (1970) and Beadle (1980), and maintains t h a t these and other authors (including Iltis himself in an earlier publication) are right about the ancestral species (teosinte) but wrong about the organ (teosinte ear) that gave rise to the maize ear. At the time of writing I am unaware of critiques of Iltis' paper except for the responses by Galinat and Mangelsdorf in letters to the editor of Science, Sept. 14, 1984; recent papers dealing with corn and its relatives have not chosen to comment on the CSTT though in some cases authors may have been unaware of Iltis' work (Walbot, 1984; Kato Y, 1984). Whatever the ultimate judgement of the CSTT and similar theories may be, at least such theories are now being taken seriously [See Gould's (1984) "Short way to corn" for perspective on the reception of ¢~hopeful monster" thinking]. Among paleobotanists Meyen (1984) has called our attention to sexual transmutations as a possibly important evolutionary mechanism. If Iltis is right about the evolution of maize, it certainly lends credence to Meyen's proposition. Stidd (1980) departed sharply from previous gradualistic explanations for the origin of Cycadeoidea (particularly the pollen bearing apparatus) and argued that neoteny was a probable mechanism [some object to treating neoteny (or heterochrony) as

123 a mechanism and prefer to think of it as a phenomenon for which a genetic/epigenetic mechanism in a strict sense is needed] that brought the relevant structures into existence abruptly and without passing through a series of morphological intermediates. Rothwell (1982) has argued similarly in attempting to account for the origin of conifers from seed ferns (as opposed to cordaites or progymnosperms). He notes the presence of two leaf types on certain pteridosperms (and Cordaites validus) and regards this heteroblastic series as evidence of heterochrony in the shoot system. He proposes that the fixation of the needle leaves in the ancestor occurred (perhaps in a single generation) in the lineage that led to conifers and that this may have resulted from heterochrony. It should be noted that Rothwell is operating here with a concept of heterochrony that is limited to a mechanism that restricts the ability of the shoot apex to the production of one type of appendage in a heteroblastic series (see Rothwell, 1982, definition on p.22). This is a simple on/offmechanism and does not include the usual component of changes in timing of development relative to other organs or relative to rate of development in ancestors and descendants. Nevertheless I applaud his breaking away from the usual gradualistic mode of explanation and entertaining alternatives involving abrupt developmental shifts. I agree with DiMichele (1985) that we are on the threshold of conceptual changes with regard to the incorporation of developmental phenomena into phylogeny reconstruction of which the examples cited above are feeble initial attempts.

Theory change To speak of conceptual change necessarily involves an understanding of background theories against which "new" ideas are judged. I have argued elsewhere (Stidd, 1985) that punctuated equilibrium and associated theories differ sharply from the concepts that prevailed during the first 2/3 of this century. Opponents counter this position in at least three ways.

Some charge that advocates of punctuated equilibrium erect a strawman - - the modern synthesis (synthetic theory) never denied stasis, sudden change, hopeful monsters, etc. Others maintain that known genetic mechanisms controlling gene frequencies in populations are sufficient to account for macroevolutionary phenomena [see Coyne and Lande's (1985) comments on Gottlieb's paper cited earlier]. Still others contend that the modern synthesis is ever expanding and incorporating "new" mechanisms and conceptual changes; Stidd is guilty of wanting to freeze and label a portion of an ongoing process of theory development. I admit to being one of the complainers Hull (1984) speaks of who regard the modern synthesis as a chameleon, infinitely malleable and capable of declaring delicious what it once found unpalatable. Hull argues that this malleability is common among scientific theories and is the result of treating conceptual systems as historical entities. So treated, a conceptual system (or a portion thereof) may evolve into its contradiction (gradually or saltatively) and still be the same system. In order to grow hypotheses must blur - - maybe so, maybe not. If Christianity were to evolve into atheism and one could identify a distinct series of intermediates, one might recognize the ensemble as the same historical entity. If the transition were accomplished abruptly one might still recognize the same entity but at the very least, for purposes of communication if nothing else, one might want to apply different labels to the pre- and posttransition phases. I prefer the Hull (1974), who I thought made a good case for replacement of one theory with another. I do not mean to imply that all attempts to explain the evolution of vascular plants based upon phyletic gradualism should be overthrown and replaced by some sort of a hybrid between punctuated equilibrium and hopeful monsters; phyletic gradualism and its legitimate offspring, telome theory, has its place, as I have argued in the beginning. My concern is that fundamentally different views on the evolution of vascular plants not be unduly

124

suppressed and my hope is that new and revealing insights into some of our longstanding problems (origin of angiosperms for instance) might be forthcoming from adoption of some of the thought patterns advocated here. As one of the reviewers of this paper has pointed out, even if one accepts abrupt morphological transitions as possible (based upon genomic and organographic restructuring) how or on what basis is the paleobotanist, in the absence of genetic information that might link divergent morphological forms, to infer non-gradualistic transitions? [Rothwell (1985) lists three criteria t h a t might suggest the sudden appearance of morphological features by heterochrony. These include: (1) ancestral taxon occurs contemporaneously in the fossil record with the derived taxon and in lower strata; (2) the ancestor exhibits in its range of mature structures those features that characterize the derived form; (3) the ancestor exhibits during its ontogeny those features that characterize the new taxon.] This is where overarching theories play an important role. The thrust of this paper is that under the modern synthesis in general and telome theory in particular, morphological gaps were traversed by "phyletic slides" and other gradualistic modes; inferences were made t h a t were in accord with gradualistic theoretical presuppositions. Saltational transitions were " o u t of style" at best if not overtly unacceptable. The plea here is for pluralism with regard to evolutionary modes and the theoretical superstructure t h a t allows alternate explanations. It has been more than 30 years now since Watson and Crick's insight into the structure of DNA. We stand on the threshold, at last, of new insights into how genomes control development in eucaryotes and how the genetic messages embedded in the genome are regulated and translated into new phenotypes. Paleobotanists can ill afford to neglect the work molecular and developmental biologists are undertaking. New books with a fresh orientation toward development such as Raft and Kaufman (1983) are highly relevant to our

concerns, which the following quote from the preface indicates. The essential position is that there is a genetic program that governs ontogeny, and that the momentous decisions in development are made by a relatively small number of genes that function as switches between alternate states or pathways. The significance of this view, if correct, is that evolutionary changes in morphology occur mechanistically, as a result of modifications of these genetic switch systems. If our prediction that there are a relatively small number of such gene switches is correct, then the potential exists for geologically rapid and dramatic evolutionary changes. Such macroevolutionary events are apparently associated with the origins of new groups of organisms.

Alas, there is almost nothing about plants or plant development in this work. To be sure, plants have distinct modes of development but many of the basic mechanisms of genome structure and regulation in animal systems should be applicable to plants. On the other hand, the modular organization of the plant body allows more flexibility than most animals possess in the topological relationships among organs. Indeterminate growth in long-lived plants allows variation in the factors that trigger the genomic events that, in turn, produce various organs at various times and positions. Paleobotanists should be aware of the phenomena of homoeosis and heterotopy (Sattler, 1974, 1985; Sattler and Maier, 1977). Plants have the ability to produce typical organs in atypical positions, though rare, morphological shifts of this type may have been of critical importance in the origin of new morphotypes leading to the establishment of new lineages and higher taxa. This potentiality creates one of the most vexing of problems for phylogeny reconstruction, tied as it is to the assessment of homologies. At least one should be aware that position is not necessarily a reliable criterion of homology. It is in this context t h a t such suggestions as gamoheterotopy gain credibility. In summary, a "new and emerging evolutionary theory" (Gould, 1980) will very likely be built around mechanisms such as: (1) a genomic (internal) mechanism for stasis; (2) the non-linear correspondence of molecular and

125

morphological evolution (maize/teosinte and humans/chimps); (3) morphological evolution driven by gene rearrangements that affect the regulatory system; (4) further elucidation of epigenetic interactions among gene products that control development; (5) increasing use of cladistic methodology to determine macroevolutionary patterns; (6) extinctions caused by major geological, climatological, or astronomical events; (7) the recognition of higher level processes, such as species selection, affecting the course of evolution. The "new" theory differs from the modern synthesis in that it utilizes a variety of mechanisms that more effectively account for macroevolutionary patterns. It is non-reductionistic in that it does not attempt to account for all macropatterns in terms of shifting gene frequencies in populations and accumulation of genes of small effect. The latter, which was at the heart of the synthesis, is relegated more or less to fine tuning after major morphological taxonomic innovations. To the extent that internally driven genomic and developmental factors are recognized as shaping macropatterns, conventional selection (Ho and Saunders, 1979) and ecological considerations play a lesser role. Major components of future evolutionary theory will be assessment of pattern (cladistics, morphology, paleontology) and genomic (internal and epigenetic) control of development as elucidated by increased understanding of genome structure at the molecular and chromosomal levels.

Acknowledgments I thank William DiMichele, Karl Niklas, and Andrew H. Knoll for their critical comments and suggestions on earlier drafts of the manuscript.

References Alberch, P., 1982. Developmental constraints in evolutionary processes. In: J.T. Bonner (Editor), Evolution and development: Dahlem Konferenzen. Springer, Berlin, 356 pp.

Arthur, W., 1984. Mechanisms of Morphological Evolution. Wiley, New York, N.Y., 275 pp. Ayala, F.T., 1983. Beyond Darwinism? The challenge of macroevolution to the synthetic theory of evolution. In: P. Asquith and T. Nickles (Editors). PSA 1982. Philos. Sci. Assoc., East Lansing, 2: 275-291. Bachmann, K., 1983. Evolutionary genetics and the genetic control of morphogenesis in flowering plants. Evol. Biol., 16:157 208. Beadle, G.W., 1980. The ancestry of corn. Sci. Am., 242: 112-119. Bonner, J.T. (Editor), 1981. Evolution and Development: Dahlem Konferenzen. Springer, Berlin, 356 pp. Brooks, D.R. and Wiley, E.D., 1986. Evolution as Entropy. Univ. Chicago Press, Chicago, Ill., 335 pp. Charlesworth, B., Lande, R. and Slatkin, M., 1982. A neoDarwinian commentary on macroevolution. Evolution, 36:474 498. Coyne, J.A. and Lande, R., 1985. The genetic basis of species differences in plants. Am. Nat., 126:141 145. DiMichele, W.A., 1985. The upward outlook in Paleobotany. Paleobiology, 11:356 359. Doebley, J.F., Goodman, M.M. and Stuber, C.W., 1984. Isoenzymatic varriation in Zea (Gramineae). Syst. Bot., 9:203 218. Doyle, J.A. and Hickey, L.J., 1976. Pollen and leaves from the Mid-Cretaceous Potomac Group and their bearing on early angiosperm evolution. In: C.B. Beck (Editor), Origin and Early Evolution of Angiosperms. Columbia Univ. Press, New York, N.Y., 341 pp. Eldredge, N. and Gould, S.J., 1972. Punctuated equilibria: An alternative to phyletic gradualism. In: T.J.M. Schopf (Editor), Models in Paleobiology. Freeman and Cooper, San Francisco, Calif., 250 pp. Foster, A.S. and Gifford, E.M., 1974. Comparative Morphology of Vascular Plants. Freeman and Cooper, San Francisco, Calif., 751 pp. Galinat, W.C., 1970. The cupule and its role in the origin and evolution of maize. Mass. Agric. Exp. Stn. Bull., 585: 1 18. Goodwin, B.C., 1984. Changing from an evolutionary to a generative paradigm in biology. In: J.W. Pollard (Editor), Evolutionary Theory: Paths into the Future. Wiley, New York, N.Y., 221 pp. Gottlieb, L.D., 1984. Genetics and morphological evolution in plants. Am. Nat., 123: 681-709. Gould, S.J., 1980. Is a new and general theory of evolution emerging? Paleobiology, 6: 119-130. Gould, S.J., 1983. The hardening of the modern synthesis. In: M. Grene (Editor), Dimensions of Darwinism. Cambridge Univ. Press, Cambridge, 336 pp. Gould, S.J., 1984. A short way to corn. Nat. Hist., 93: 12-20. Heberer, G. (Editor), 1943. Die Evolution der Organismen. Ergebnisse und Probleme der Abstammungsgesehichte. Fischer, Jena, 754 pp. Hilu, K.W., 1983. The role of single-gene mutations in the evolution of flowering plants. Evol. Biol., 16:47 122.

126 Ho, M.W. and Saunders, P.T., 1979. Beyond neo-Darwinism -- an epigenetic approach to evolution. J. Theor. Biol., 78:573 591. Hull, D.L., 1974. The Philosophy of Biological Sciences. Prentice-Hall, Englewood Cliffs, N.J., 148 pp. Hull, D.L., 1984. Cladistic theory: Hypotheses that blur and grow. In: T. Duncan and T.F. Stuessy (Editors), Cladistics: Perspectives on the Reconstruction of Evolutionary History, Columbia Univ. Press, New York, N.Y., 312 pp. Iltis, H.H., 1983. From teosinte to maize: the catastrophic sexual transmutation. Science, 222:886 894. Kato Y, T.A., 1984. Chromosome morphology and the origin of maize and its races. Evol. Biol., 17: 219-253. Kauffman, S.A., 1983. Developmental constraints: internal factors in evolution. In: B.C. Goodwin, N. Holder and C.W. Wylie (Editors), Development and Evolution. Cambridge Univ. Press, London, 437 pp. King, M.C. and Wilson, A.C., 1975. Evolution at two levels in humans and chimpanzees. Science, 188: 107-116. Kollar, E.J. and Fischer, C., 1980. Tooth induction in chick epithelium: expression of quiescent genes for enamel synthesis. Science, 207: 993-995. Meyen, S.V., 1984. Gamoheterotopy - - a probable process in the morphological evolution of higher plants. Int. Org. Palaeobot. Newsl., 25: 4-5. O'Grady, R.T., 1984. Evolutionary theory and teleology. J. Theor. Biol., 107: 563-578. Raft, R.A. and Kaufman, T.C., 1983. Embryos, Genes and Evolution. Macmillan, New York, N.Y., 395 pp. Reif, W.E., 1983. Evolutionary theory in German paleontology. In: M. Grene (Editor), Dimensions of Darwinism. Cambridge Univ. Press, London, 336 pp. Rothwell, G.W., 1982. New interpretations of the earliest conifers. Rev. Palaeobot. Palynol., 37: 7-28.

Rothwell, G.W., 1985. The role of heterochrony in vascular plant evolution. Am. J. Bot., 72(6): 887. Sattler, R., 1974. A new conception of the shoot of higher plants. J. Theor. Biol., 47:367 382. Sattler, R., 1985. Ontogenetic and phylogenetic implications of homoeosis. Am. J. Bot., 72(6): 831. Sattler, R. and Maier, V., 1977. Development of the epiphyllous appendages of Begonia hispida var. cucullifern: Implications for comparative morphology. Can. J. Bot., 55: 411-425. Schindewolf, O.H., 1936. Pal~iontologie, Entwicklungslehre und Genetik. Kritik und Synthese. Borntraeger, Berlin, 108 pp. Schindewolf, O.H., 1950. Grundfragen der Pal/iontologie. Schweizerbart, Stuttgart, 506 pp. Simpson, G.G., 1944. Tempo and Mode in Evolution. Columbia Univ. Press, New York, N.Y., 237 pp. Stewart, W.N., 1983. Paleobotany and the Evolution of Plants. Cambridge Univ. Press, New York, N.Y., 405 pp. Stidd, B.M., 1980. The neotenous origin of the pollen organ of the gymnosperm Cycadeoidea and the implications for the origin of higher taxa. Paleobiology, 6:161 -167. Stidd, B.M., 1985. Are punctuationists wrong about the modern synthesis? Philos. Sci., 52: 98-109. Waddington, C.H., 1975. The Evolution of an Evolutionist. Cornell Univ. Press, Ithaca, New York, N.Y., 328 pp. Walbot, V., 1983. Morphological and genomic variation in plants: Zea mays and its relatives. In: B.C. Goodwin, N. Holder and C.C. Wylie (Editors), Development and Evolution. Cambridge Univ. Press, London, 437 pp. Yunis, J.J. and Prakash, O., 1982. The origin of man: a chromosomal pictorial legacy. Science, 215: 15251530. Zimmermann, W., 1930. Phylogenie der Pflanzen. Fischer, Jena, 452 pp.