Chapter 7 Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited Richard N\. Bateman and William A. D/M/che/e ABSTRACT Further developing a controversial neoGoldschmidtian paradigm that we first pub- lished in 1994, we here narrowly define saltational evolution as a genetic modifica- tion that is expressed as a profound phenotypic change across a single generation and results in a potentially independent evolutionary lineage termed a prospecies (the 'hopeful monster' of Richard Goldschmidt). Of several saltational and parasaltational mechanisms previously discussed by us, the most directly relevant to evolutionary-developmental genetics is dichotomous saltation, which is driven by mutation within a single ancestral Uneage. It can result not only in instantaneous speciation but also in the simultaneous origin of a profound phenotypic novelty more likely to be treated as a new supraspecific taxon. Saltational events form unusually long branches on morphological phylogenies, which follow a punctuated equilibrium pattern, but at the time of origin they typically form zero length branches on the contrastingly gradualistic molecular phylogenies. Our chosen case- studies of heterotopy (including homeosis) and heterochrony in fossil seed-ferns and extant orchids indicate that vast numbers of prospecies are continuously generated by mutation of key developmental genes that control morphogenesis. First principles suggest that, although higher plant mutants are more likely to become established than higher animals, the fitness of even plant prospecies is in at least most cases too low to survive competition-mediated selection. The establishment of prospecies is most Hkely under temporary release from selection in environments of low biotic competition for resources, followed by honing to competitive fitness by gradual rein- troduction to neoDarwinian selection. Unfike neoDarwinism alone, this two-phase evolutionary paradigm is consistent with the recent results of (a) whole-genome sequencing, which have revealed a surprisingly small total number of genes per model species, and (b) of Quantitative Trait Locus analyses, which indicate that major phenotypic features are determined by one or two homeotic genes of major phenotypic effect and only a handful of genes of lesser effect. Evolutionary- developmental genetics has already proved beyond reasonable doubt the credibility of the initial 'generative phase' of the neoGoldschmidtian hypothesis (though further investigation is needed of the effects of canalisation and epigenesis following both gain and loss of function). Unfortunately, far fewer data are currently available to test the subsequent 'estabhshment phase'; this deficiency places a premium on moni- toring the ecological progress of many prospecies, in both artificial and natural In Develojmwntal Genetics and Plant EiKilution (2002) (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 109-159. 110 R. M. Bateman and W. A. DiMichele habitats. Saltation is superior to classical neoDarwinian selection in removing the highly improbable requirement to drive alleles to fixation in large populations, explaining sympatric speciation, allowing lineages to cross otherwise lethal fitness valleys, giving key evolutionary roles to pre-adaptation and exaptation rather than adaptation, and providing a direct causal explanation of the qualitatively different levels of morphological divergence that underpin the Linnaean hierarchy. 7.1 Introduction On the theory of natural selection we can clearly understand the full meaning of that old canon in natural history, 'Natura non facit saltum.' This canon, if we look only to the present inhabitants of the world, is not strictly correct, but if we include all those of past times, it must by my theory be strictly true. (Jones, 1999: 189) In the summer of 1993, we attempted to synthesise a new 'supraDarwinian' paradigm in the evolutionary biology of vascular plants for an edited volume entitled Shape and Form in Plants and Fungi (Bateman and DiMichele, 1994a). Our wide-ranging discus- sion primarily concerned the credibility of, and the evidence for, non-gradual evolu- tion of plant form that did not rely on classic neoDarwinian mechanisms - in other words, on directional or disruptive selection acting via adaptively-driven fixation of mutant alleles and traced via Hardy-Weinberg equilibria within large panmictic popu- lations (for clear expositions of these principles see Ridley, 1996; Patterson, 1999). We ultimately reached the following conclusions (p. 91): It has long been accepted that the fundamental unit of evolutionary change is the gene but that such changes are mediated via the phenotype of the host organism (the replicators and interactors respectively of Dawkins, 1982, 1986, 1989). Recent studies of [homeotic] gene expression in plants (e.g. Coen, 1991; Coen and Carpenter, 1992; ...) provide a vital causal link between genotype and phenotype - replicator and interactor - that allows reciprocal illumination between these two contrasting manifestations of the evolutionary process. [Attributes of homeotic] genes can be coded cladistically in order to make the crucial distinction between primitive and derived states and, as we have shown, the resulting cladograms can be used to test competing hypotheses of underlying evolutionary mechanisms. Despite recent advances (Chasan, 1993), biologists have been surprisingly slow to combine relevant concepts of gene expression, developmental control, phylogeny reconstruction, ecological filtering of pheno- types, and evolutionary theory into a truly integrated evolutionary synthesis. This problem has been exacerbated by over-enthusiastic generalisation from parochial studies of a few 'flagship' species to ail-embracing evolutionary theo- ries. Nonetheless, we are confident that future syntheses will confirm our opinion that plants have their own distinct approach to the evolution of shape and form. These deUberately provocative statements, and our subsequent reformulations of various aspects of the paradigm (Bateman, 1994, 1996, 1999a, b; Bateman and -1 Saltational evolution I I I DiMichele, 1994b; DiMichele and Bateman, 1996; Bateman et al., 1998) attracted disappointingly few commentaries (e.g. Rutishauser, 1995; Erwin, 2000; Tucker, 2000, 2001) prior to this volume (Baum and Donoghue, 2002; Cronk, 2002; Theis- sen et al., 2002). Our 1994 synthesis was very much a product (or perhaps a victim?) of its time. Despite a few eloquent dissidents, often from the palaeobiologi- cal community (most notably Gould and Lewontin, 1979; cf. Morris, 2001), evolu- tionary theory was (and is) dominated by strict neoDarwinians whose perspectives differed only in fine detail: all relied on the mathematically modelled gradual spread through populations of alleles that engendered subtle modifications of phenotype, increasing in frequency through directional or disruptive selection mediated primar- ily by competition (for recent examples, the latter extensively quoted in this chapter, see Dawkins, 1986, 1989; Maynard Smith, 1989; Maynard Smith and Szathmary, 1995; Ridley, 1996; Jones, 1999). Adaptation was used, often unthinkingly, as a null hypothesis for most specific evolutionary transitions (Bateman and DiMichele, 1994a) and for evolutionary radiations (Bateman, 1999a), however limited and ambiguous the evidence for levels of selection capable of inducing genuine specia- tion. And botanists had surprisingly little to say on such lofty matters, preferring to co-opt, with at best minor modifications, theories that were essentially zoocentric. However, in the field of developmental genetics, genuine breakthroughs in under- standing the control of metazoan body plans through the homeotic Hox genes (e.g. Slack et al., 1993; Valentine et al., 1999; Mindell and Meyer, 2001) had been accompanied by the elucidation of the classic ABC model of angiosperm flower development through studies of Arabidopsis and Antirrhinum (e.g. Coen and Meyerowitz, 1991; Theissen et al., 1996, 2002; Cubas, 2002). Also, the increasingly perceived possibility of harnessing these emerging insights in developmental genetics for evolutionary studies prompted the benchmark plant evo-devo conference at Taos, New Mexico in the summer of 1993 (summarised by Chasan, 1993, as cited by us in the above quote). Eight years on, it seems appropriate to assess how much (or indeed how little) progress has been made toward the crucial goal of formulating a holistic evolution- ary paradigm that encompasses the origin, phylogenetic context and ecologically- mediated fates of mutations in key morphogenetic genes. 7.2 SupraDarwinian evolutionary mechanisms 7.2. / NeoGoldschmidtian saltation Geneticists were once so impressed with mutation as to suggest that new forms of life arise not through the accumulation of small changes but in great leaps. Evolution was due to the instability of genes and genetics had, perhaps, destroyed Darwin's idea. It had not: mutation is the fuel rather than the engine of biological advance. The process involves mechanisms undreamed of in the science's first days. (Jones, 1999: 147) In his notorious evolutionary tome The Material Basis of Evolution, the Berkeley- based developmental zoo-geneticist Richard Goldschmidt (1940) argued that 112 R. M. Bateman and W. A. DiMichele 'systemic mutations' (large-scale chromosomal rearrangements) altered early W^,. developmental trajectories to generate, across a single generation, 'hopeful monsters' % - teratological lineages of phenotypes radically different from their parents. By i,, chance, some hopeful monsters possessed high levels of fitness that enabled their |.? persistence as new lineages of great evolutionary significance. It was not difficult for S aggressive advocates of the neoDarwinian New Synthesis to fatally undermine Gold- ^,^- Schmidt's thesis by discrediting his concept of macromutations and mathematically |^<| 'proving' the improbability of hopeful monsters instantaneously acquiring competi- |: tively high fitness. Consequently, occasional attempts to resurrect various aspects of % Goldschmidt's saltational paradigm (e.g. Waddington, 1957; Croizat, 1962; van ^^ Steenis, 1976; Gould, 1982; Arthur, 1984; Orr, 1991; Bateman and DiMichele, ^') 1994a), or to re-assess the generally overlooked contributions of Goldschmidt's '?'?? intellectual predecessors (e.g. see the discussion of the views of influential German 1% plant morphologist W. Troll as portrayed by Kaplan, 2001b), attracted relatively g^ little attention. ^'t As few evolutionary biologists provided explicit definitions of saltational (or 'saltatory') evolution, the term has been used to encompass a wide range of often . .^, J conflicting concepts. In our previous attempt to define (and thus recognise) salta- /f'i" tional evolutionary events (Bateman and DiMichele, 1994a), we immediately excluded from consideration all non-genetic ecophenotypic and ontogenetic vari- ^^| ation within species. We also emphasised the related difference between the concept of a teratos - an individual possessing a radically different morphology from its immediate ancestor(s) irrespective of the underlying causal mechanism - and Gold- schmidt's concept of a 'hopeful monster', where a genetic cause of the morpho- logical discontinuity is assumed and non-heritable causes arc specifically excluded ^^ (Table 7.1). Saltation requires a substantial change in phenotype between ancestor and j. descendant. As developmental genetic studies have conclusively demonstrated that ; Table 7. / Formal definitions of key terms relating to exceptionally rapid speciation (modified after '':^.,] Bateman and DiMichele, 1994a: 66-67) "t'\ Saltation: a genetic modification that is expressed as a profound phenotypic change across a single n > generation and results in a potentially independent evolutionary lineage. .^ ' Porasaltation: a genetic modification that is expressed as a profound phenotypic change across two '|, , to several generations and results in a potentially independent evolutionary lineage. ,^' * Dichotomous saltation: saltation driven by mutation of at least one gene v^ithin a single ancestral 3| (t lineage. '^; Reticulate saltation: saltation driven by allopolyploidy and thus blending the entire genomes of two || ancestral lineages. t- Teratos: an individual showing a profound phenotypic change from its parent(s) irrespective of whether the underlying cause is genetic or ecophenotypic (plural, terato). Hopeful monster: an individual showing a profound phenotypic change from its parent(s) that demonstrably reflects a genetic modification. Taxonomic species: one or more (typically many more) populations separated from all other comparable populations by phenotypic, and putative genotypic, discontinuities that are believed to reflect one or more isolating mechanisms operating over a considerable period of time. Prospedes: a putatively recently evolved lineage possessing the essential intrinsic properties of a taxonomic species but yet to achieve levels of abundance and especially of longevity acceptable to practising taxonomists. t Saltational evolution 113 magnitude of phenotypic change engendered by a modification of a specific gene is decoupled from the magnitude of the change in the genome itself, quantification of the degree of phenotypic change is clearly the most appropriate criterion for salta- tion. Increased overall complexity is definitely not a requirement; indeed, current evidence suggests that saltational events which suppress developmental genes and consequently reduce morphological complexity are far more common than salta- tional events which increase overall complexity (cf. Kellogg, 2002). In 1994 we abrogated our responsibility to define the profoundness of morpho- logical transition necessary to pass the threshold of saltation, and we continue to do so here. The primary expectation is of a high degree of phenotypic divergence in a well-sampled phylogenetic (and perhaps phenetic: DiMichcle et ai, 2001) study that allows reasonably accurate comparison of degrees of morphological divergence, which should be considerable, and of sequence divergence, which should be minimal in the immediate aftermath of the saltation event but, unlike morphology, changes progressively and gradually thereafter (Bateman, 1999a). Rate of evolutionary change is a second key criterion for saltation. Some authors (e.g. Ayala and Valentine, 1979) chose to define saltation as a period when the tem- poral rate of evolution (change/time) is substantially greater than the long-term average within the lineage. However, this definition is more appropriately discussed in the context of evolutionary radiations (Bateman et al., 1998; Bateman, 1999a), as it encompasses not only our saltation s.s. but also several contrasting mechanisms of rapid evolutionary change that we prefer to collectively term 'parasaltational' (see Section 7.2.2). We believe that saltation is better defined by generation time than absolute time, and hence argue that a saltational change must occur across a single generation. Although hopeful monsters will have a much greater likelihood of retaining their novel phenotype if they become reproductively isolated from the parental population, particularly if the isolation reflects intrinsic properties of the monsters rather than mere ad hoc spatial separation (i.e. sympatry rather than allopatry), new lineages can in theory become established even in the absence of reproductive isolation (Arthur, 1984). This criterion is therefore ancillary to, rather than inherent in, saltation, which can now be defined more precisely as a genetic modification that is expressed as a profound phenotypic change across a single gen- eration and results in a potentially independent evolutionary lineage (Table 7.1). A single hopeful monster has by definition a minimal geographical and ecological distribution; if also reproductively isolated, in principle it fulfils the criteria required for a biological species sensu Mayr (1963). However, in practice the hopeful monster is unlikely to be awarded specific rank by a taxonomist, who requires a taxo- nomic species to demonstrate a degree of historical tenacity by establishing a size- able population that persists through many generations. This is a reasonable modus operandi, as most lineages resulting from saltation undoubtedly fail to survive beyond a single generation, and very few exceed ten or a hundred generations; these typically ephemeral entities are better described as prospecies (Table 7.1). Note that there is no intrinsic biological distinction between prospecies and taxonomic species; taxonomic species can only be distinguished retrospectively, on the basis of their far greater temporal continuity and spatial extent. Also, an ageist bias is evident in most taxonomic treatments. A species inevitably has an origin, an acme and ultimately an extinction that are defined both temporally and spatially (Levin, 2000, 2001). I 14 R. M. Bateman and W. A. DiMichele ANCESTRAL SPECIES DESCENDANT SPECIES ANCESTRAL SPECIES A DESCENDANT SPECIES (a) morphogenetic mutation (b) ANCESTRAL SPECIES B allopolyploidy ANCESTRAL SPECIES DESCENDANT SPECIES directional selection or drift SPECIES A SPECIES B (ancestor-descendant assumptions not made) (0 isolation m (unspecified process) Figure 7.1 Comparison of contrasting evolutionary patterns. Dichotomous saltation (a) shows Instantaneous divergence of descendant from ancestor via a mutation in a key gene con- trolling morphogenesis. Reticulate saltation (b) also occurs instantaneously via allopoly- ploidy but blends two parental genomes. Directional selection or drift (c) cause gradual divergence of the descendant following its isolation. Cladistic representations of specia- tion (d) assume no ancestor-descendant relationships and specify no underlying process. However, in practice, taxonomists are more reluctant to recognise as a full species a rare but putatively recent, expanding population than a rare but putatively long- lived, senescent population that represents far greater historical continuity. Thus far, we have considered only mutationaily-driven saltation. Other modes of genotypic change rely on mixing pre-existing genes from individuals of two species (hybridisation) or on duplicating a complete set of pre-existing genes in a single indi- vidual (autopolyploidy), but neither phenomenon generates a new reproductively Saltational evolution 115 Table 1.1 Examples of parasaltational evolutionary mechanisms, v^ith relevant literary sources (a) Reticulate processes that combine formerly disparate lineages I. Hybridisation* 2. Endosymbiosis Stace, 1989, 1993; Goodnight, 1995, 1999; Rieseberg et al., 1995; Wendel ef o/., 1995; Rieseberg, 1997; Vogel et o/., 1999; Rieseberg and Burke, 2001 Margulis, 1993; Martin and Schnarrenburger, 1997 (b) Processes intrinsic to the behaviour of the genome 3. Homeosis* 4. Neutral theory 5. Nearly neutral theory 6. Adaptive mutation 7. Molecular drive 8. Meiotic drive 9. Multiple codes 10. Chromosomal rearrangements 11. Transposon-induced deactivation Raff and Kauffman, 1983; Arthur, 1984, 2000; Kauffman, l993;Wray, 1995; Albert eto/., 1998 Kimura, 1983, 1991 Ohta. 1992, 1995 Foster and Cairns, 1992; Shapiro, 1997, 2002 Dover, 1982,2000 Pomiankowski and Hurst, 1993; McVean and Hurst, 1997 Trifonov, 1997 Prescott and DuBois, 1996; Hoffman and Prescott, 1997 Wessler et al., 1995; Federoff, 2000; Walbot, 2002 (c) Processes emergent from genetic control of development 12. Epigenesis 13. Epistasis Goodwin and Saunders, 1992; Jablonka et o/., 1992; Goodwin, 1994; Jablonka, 1994; Jablonka and Lamb, 1995 Papers in Wolf et o/., 2000 (d) Processes direaly linked to the ecological spread of genetic novelties 14. Drift 15. Shifting balance 16. Correlated selection 17. Species selection 18. Clade selection Note; * = events that are also potentially saltational. Templeton, 1989; Gillespie, 1991; Barrett and Pannell, 1999; Patterson, 1999 Wade, 1992; Goodnight, 1995; Whitlock, 1997; Wade and Goodnight, 1998; Mallet and Joron, 1999 Price et o/., 1993 Gould, l986;Eldredge, 1989 Williams, 1992 I 16 R. M. Bateman and W. A. DiMichele isolated evolutionary lineage across a single generation. However, by first mixing genes of two lineages and then duplicating the entire heterogeneous genome, thus restoring fertility, allopolyploidy does immediately generate a novel lineage that is often also reproductively isolated (Stebbins, 1971; Stace, 1989, 1993; Thompson and Lumaret, 1992; Wendel et al., 1995; Rieseberg, 1997; Vogel et ai, 1999; Riese- berg and Burke, 2001; Wolfe, 2001). Similarly, the endosymbiotic origins of mito- chondria and plastids (Margulis, 1993; Martin and Schnarrenberg, 1997) can only reahstically be viewed as unusually profound reticulate saltation events. Thus, Bateman and DiMichele (1994a) concluded that two distinct modes of saltation exist (Table 7.1, Figure 7.1). In dichotomous saltation (Figure 7.1a), hopeful monsters originate by mutation; one new daughter lineage diverges instanta- neously from the ancestral lineage, thereby forming a dichotomous pattern that can in theory be resolved cladistically (as can the gradual divergences implicit in direc- tional selection or drift: Figure 7.1c). However, in reticulate saltation (Figure 7.1b), allopolyploidy combines elements from two ancestral lineages; the resulting reticu- late pattern cannot be adequately accommodated in a dichotomous cladogram (note that the cladistic method is neutral regarding both ancestor-descendant and process- based interpretations: Figure 7. Id). The general absence of mutation in reticulate saltation restricts the potential range of immediate phenotypic innovation, so that speciation events are less likely to coincide with the origins of supraspecific taxa than is the case in dichotomous saltation (cf. van Steenis, 1976; Arthur, 1984; Stace, 1993; Wolfe, 2001). Thus, dichotomous saltation is of greater relevance to evolu- tionary-developmental genetics, though reticulate saltation also remains an import- ant evolutionary process as each such event is on average more likely to generate viable phenotypes capable of establishing long-lived lineages. 7.2.2 The diversity of parasaltational mechanisms Quite how [mimetic] insects traversed the valley of death - in a sudden leap, with a single gene pushing them most of the way, or by small changes getting together by accident - is not clear. (Jones, 1999: 160) The narrowness of our definition of saltation excludes several evolutionary mechan- isms, most under-explored, which are capable of causing speciation events that are exceptionally rapid but not instantaneous. These are more appropriately described as parasaltational (Table 7.1). First, the stringent requirement for both genotypic and phenotypic change across a single generation excludes from strict saltation most mutations of recessive alleles; here, the genotypic change can only be expressed in the Fl generation in rare cases where a recessive mutation in a germ cell precursor is followed by self-fertilisation involving two gametes, each of which carries the mutation (Arthur, 1984). Hybridis- ation per se is similarly excluded (cf. Abbott, 1992; Rieseberg et ai, 1995). Specifying instantaneous speciation also rules out evolutionary scenarios that focus on populations of small effective sizes, typically due to reduction induced by various forms of environmental stress, by a marginalisation event leading to para- patry, or by a vicariance event leading to allopatry (Levinton, 1988). The neutral Saltational evolution I 17 theory (Kimura, 1983, 1991) and subsequent nearly neutral theory (Ohta, 1992, 1995) predict that random sampling effects alone can lead to allele fixation or extinction in small populations, largely independent of selective advantage. Various reformulations of Wright's (1932, 1968) shifting balance theory (Lewis, 1962, 1966, 1969; Levin, 1970, 1993, 2000; Templeton, 1982, 1989; Carson, 1985; Lande, 1986; Wade, 1992; Whitlock et al., 1995; Whitlock, 1997; Wade and Goodnight, 1998; Mallet and Joron, 1999; Wolf et al., 2000; cf. Coyne et al., 1997) predict that random genetic drift in small populations can temporarily override selective pres- sures on alleles, thereby allowing populations to cross non-lethal valleys on the adaptive landscape to the slopes of another peak, which is then climbed by classic neoDarwinian selection. Drift is in theory expressed most profoundly when it dis- rupts and destabilises developmental homeostasis (Levin, 1970; see also Patterson, 1999). Although most such populations fail, this process provides an occasional opportunity to substantially re-organise the developmental programming under con- ditions of low infraspecific competition and high physical stress ('catastrophic selec- tion' sensu Lewis, 1962, 1966, 1969; Carson, 1985). Shifting balance scenarios are consistent with evolutionary patterns that were termed 'punctuated equilibria' by Eldredge and Gould (1972) - long periods of stasis followed by brief periods of rapid phenotypic change. Vermeij (1987) extended the ecological component of these scenarios, arguing that periods of stasis reflect neoDarwinian processes and are punctuated by ecosystem disruptions that locally reduce selection pressure, species diversity and population sizes. Each such disruption allows escalation - a brief interval of intense competition to fill the vacated niches that increases the fitness of the competitors. Many of these observa- tions apply equally well to populations that are very small, not because they have recently declined into an apocryphal 'bottleneck' but because they have just evolved by saltation - we will return to them later. Other explanations of punctuational pat- terns require differential survival of lineages, focusing on selection among species (Gould, 1986; Levinton, 1988; Gould and Eldredge, 1993) or even among clades (Williams, 1992). 7.3 Cladistic tests of evolutionary hypotheses Cladistics, a German invention, has strict rules and a complex vocabulary. It can, if not carefully used, give erratic results and is still filled with argument about just what should be plugged into its analyses. It has, nevertheless, trans- formed our view of the world. (Jones, 1999:371) In 1994, we felt obliged to outline the basic principles and methodology of cladistics before discussing its relevance to saltation theory. Presenting this background is no longer necessary, given the pre-eminence since achieved by cladistic techniques for reconstructing phylogenies. However, it is worthwhile restating our suggested use of cladograms for falsifying saltational hypotheses, and reviewing cladistic falsification of adaptation and exaptation in the light of increasing use of mapped quantitative variables for ecological interpretations (see review volumes by Harvey and Pagel, 1991; Harvey et al., 1996; Silvertown et al., 1997). Also, the rapid and profound 118 R. M. Bateman and W. A. DiMichele switch during the last decade from cladistic analyses based on morphology to those based on increasingly profligate DNA sequence data requires further consideration (cf. Bateman, 1999a; Chase et ai, 2000). Phylogenies can in practice be recon- structed using sequence data alone, but evolution can be understood only by relating genotype explicitly to phenotype. 7.3. / Falsification of adaptation and exaptation The number of morphological cladistic analyses of plants leading to interpretations of underlying causal mechanisms remains surprisingly small; numbers began to rise during the 1990s, but then plateauxed as sequence matrices replaced morphology. Most such examples focused on adaptation (for early examples see Coddington, 1988; Donoghue, 1989; Maddison, 1990; for reviews see Harvey and Pagel, 1991; Harvey et ah, 1996; Silvertown et ai, 1997), and require three important codicils: 1 Many traits are likely to be adaptive (increase the perceived overall fitness of the organism) but far fewer are identifiable as adaptations that evolved via natural selection to fulfil a specific function. Despite many published criticisms, this key distinction is still often overlooked. 2 Morphological cladistic analyses by definition employ 'form' as characters, but rarely include explicit functions (cf. Lauder, 1990). Fortunately, this is not a serious handicap to interpretation, as particular functions can be plotted on a ciadogram a posteriori (we discuss this procedure, strictly termed 'mapping', in more detail below). 3 When attempting to infer evolutionary process from cladistic pattern, it is only possible to state that a particular evolutionary process is consistent with a particular phylogenetic pattern. Demonstrating such a correlation requires addi- tional biological data that are not appropriate for coding into the original cladistic matrix. To be consistent with a hypothesis of adaptation, a particular form (represented as one or more character-state transitions on the morphological ciadogram) and a particular function (mapped a posteriori) must evolve on the same branch of the ciadogram. A form appearing below the postulated function on the ciadogram is consistent with a hypothesis of exaptation; the form either evolved non-adaptively, or evolved adaptively but for a different function, only later acquiring its present function. A form appearing above the putative function on the ciadogram refutes the hypothesis of positive correlation and thus of any causal relationship. Arrangements of form and function consistent with adaptation or exaptation are not positive proof of such hypotheses; rather, the value of the cladograms is negative, allowing falsifi- cation of postulated correlations. 7.3.2 Falsification of transference of function This logic of transitional correlation also underpins the test of transference of func- tion proposed by Baum and Donoghue (2002; also D. Baum, pers. comm. 2001), where the phylogenetic distribution of a particular function is mapped relative to Saltational evolution 119 two or more non-homologous structures known to fulfil the function across the clade under scrutiny. Polymorphism of function in the hypothetical ancestor, or the presence of species where neither structure fulfils the function in question, both refute the hypothesis of transfer of that function from one structure to the other during the evolution of the clade. As with tests of adaptation and exaptation, the a priori hypothesis is conclusively refuted by a negative correlation, but is not proven by a positive correlation. 7.3.3 Falsification of saltation Bateman and DiMichele (1994a) adopted and amended the logic of phylogenetic fal- sification to develop a cladistic test of non-adaptive, saltational hypotheses. The emphasis switches from demonstrating the simultaneous origin of a character state and its presumed adaptive function to demonstrating the simultaneous origin of several developmentally correlated character states. This, in turn, focuses attention on long branches - those supported by several morphological character-state transi- tions - and requires a literal (and thus somewhat philosophically controversial) interpretation of the ciadogram as an evolutionary history. In this scenario, poten- tially developmentally correlated characters changing simultaneously on the dado- gram are assumed to have changed simultaneously during evolution, most probably as the direct or indirect consequence of a single mutation event. In other words, saltation is regarded as the null hypothesis to explain particular long branches in morphological cladograms. The credibility of this test is heavily dependent on the density of species sampling. Ideally, all known species in the chosen clade, both extant and extinct, should be sampled and coded in order to maximise the probability of dissociating multiple character-state transitions on a single branch. A more pragmatic approach would be to analyse the readily obtained species initially and then add other relevant species as they become available, as a secondary test of the initial saltational hypothesis (Bateman and DiMichele, 1994a, Figure 3). There are several potential difficulties with using long branches in morphological trees as circumstantial evidence of saltation events: 1 Some manuals of morphological cladistic analysis state that morphological char- acters which are potentially developmentally correlated fail the cladistic require- ment for independence and hence should be reduced to a single character prior to tree-building. If effectively implemented, this procedure would eliminate any potential insights into developmental correlation. However, the complexities of developmental genetics mean that this is not a practical recommendation; many phenotypic characters are demonstrably under highly polygenic control, while single key genes frequently regulate many features of an organism (pleiotropy). The best approach to coding a species for morphological cladistic analysis is to describe as many features as possible that can be delimited and can reasonably be assumed to be under genetic control, leaving developmental correlation to be assessed a posteriori. 2 Long branches tend to be especially mutually attractive during tree-building, often yielding incorrect topologies (long-branch effects: e.g. Hendy and Penny, 120 R. M. Bateman and W. A. DiMichele 1989); in such cases the long branch will no longer be present to be examined for evidence of saltation, having been substantially shortened in order to insert the long-branch taxon into an incorrect position on the cladogram. 3 Even if sampling of known species is maximised, long morphological branches could still reflect at least two non-saltational evolutionary scenarios. First, they could be due to the absence (most commonly by extinction) of several phyloge- netically intermediate species. Second, it could conceivably reflect the acquisition of several phenotypic characters by a lineage in the absence of any divergent speciation (i.e. by anagenesis). Although there is limited direct evidence that anagenetic evolution takes place (but see Section 7.7.2), equally it is difficult to demonstrate that the observed character-state transitions accompanied a single speciation event. 7.4 Punctuated equilibria in morphology, plus phyletic gradualism in DNA sequences, equals evolution That morphological and genetic changes are not always parallel seems entirely reasonable at first, but this statement must be tempered by the fact that estab- lishing the extent of 'great morphological change' is highly subjective. Like 'key' characters, it is likely to be influenced by a single novelty that we view as significant because it epitomises a highly successful group of plants. The import- ance of such single novelties must be viewed against the backdrop of the major- ity of traits still shared by all taxa due to overall genetic similarity ... Statements like 'rapid radiations are from first principles better tracked by mor- phology than molecules' (Bateman, 1999: 432) are based on the assumption that specific novelties are adaptive and successful from the onset. Individual novelties only appear important because we know that particular groups are successful today. At the time when they first evolved, such novelties would not be highly significant because the overall genetic environment would still have been similar to that of their close relatives. (Chase et ai, 2000: 166-167) The 1990s were also characterised by ongoing debates regarding whether the punc- tuational pattern of evolution perceived and widely popularised by S. J. Gould, N. Eldredge and others (Eldredge and Gould, 1972; Gould and I.ewontin, 1979; Eldredge, 1992; Gould and Eldredge, 1993) was real, rather than an artefact of the absence from the fossil and living records of a myriad of phylogenetically intermedi- ate species ('ghost' species that would reflect non-preservation due to rapid extinc- tion, persistent rarity and/or relatively poor preservation potential). Recent reviews of the completeness of the fossil record strongly suggest that the proportion of animal species that ever existed that are preserved in the fossil record is greater than all but the most optimistic palaeontologists had predicted (Donovan and Paul, 1998); it is less clear whether this statement applies equally well to plants. The best-documented case studies of morphological evolution in the animal fossil record (e.g. Wray, 1995; Jackson and Cheetham, 1999) give great credibility to the reality of the rectangular, phenogram-like pattern inherent in punctuated equilib- rium (Figure 7.2a). Furthermore, review of the recent literature suggests that the Saltational evolution 121 MORPHOLOGY 1 t E -5 UI Z h- (a) SEQUENCE DIVERGENCE (arithmetic) DIVERGENCE (arithmetic) Figure 7.2 A simple hypothetical phylogeny of eight species, four extant and four extinct, all ulti- mately derived from a single ancestor. Evolutionary patterns are contrasted for morpho- logical data (a), showing geologically instantaneous (punctuational) morphological divergence, and sequences from non-morphogenetic regions of the genome (b), showing constant, clock-like sequence divergence. In this example both speciation events and extinction events are roughly evenly spaced and the magnitude of morphological diver- gence is random through time; features that maximise the likelihood of correctly recon- structing the phylogeny of the clade (Bateman, 1999a). Note that molecular data cannot determine the relationships of the four extinct species, nor can they separate the most recently divergent of the four extant species from its sister-species (in this example, there has been insufficient time for the novel species to acquire molecular autapomor- phies). Also, had the earlier divergences of the three molecularly distinguishable extant lineages been more closely spaced in time (i.e. had they constituted a bona fide radiation), we would have been far more likely to satisfactorily resolve their relationships through morphological than through sequence data (modified after Bateman, 1999a, Figure 19.2a, b; see also Bateman, 1996, 1999b). reality of long periods of evolutionary stasis in specific lineages (i.e. 'equilibrium') is increasingly accepted by both neoDarwinian and supraDarwinian researchers. Bateman (1999a) argued that the most obvious explanation for stasis is that, in most ecological circumstances, neoDarwinian natural selection enhances phenotypic stability. In other words, the background mode of natural selection is stabilising selection, which inhibits evolutionarily meaningful morphological change. The relat- ively rapid intervening periods of evolution and speciation (i.e. 'punctuation') may occur under the relatively high directional or disruptive selection pressures that underpin neoDarwinian microevolution, or alternatively they may occur even more rapidly under the relatively low selection pressures that are more characteristic of 122 R. M. Bateman and W. A. DiMichele the various supraDarwinian macroevolutionary scenarios outlined above. In either case, the morphological divergence appears geologically instantaneous. However, non-fossil phylogenetics was increasingly dominated through the 1990s by DNA sequence phylogenies for regions of the genome that are either non-coding or code for various biochemical pathways that are not morphologically expressed. There are reasons to assume that such regions of the genome have broadly clock-like properties, even if the clock is somewhat unreliable (e.g. Avise, 1994; Sanderson, 1997, 1998). It has become conventional wisdom that, at least in most circum- stances, phylogenetically favoured regions of the genome such as plastid genes (Chase and Albert, 1998) and nuclear ribosomal genes (Hershkovitz et ai, 1999) accumulate non-lethal mutations with the semi-regularity of a Geiger counter (admittedly, evidence continually accrues of clear contraventions of this 'steady state'). Thus, first principles suggest that these sequence data change by something approaching phyletic gradualism (Figure 7.2b). Hence, rather than being alternative patterns of evolutionary change that justifi- ably engender keenly-fought arguments among evolutionary theorists, evolution typically occurs via both punctuated equilibria (morphology) and phyletic gradual- ism (DNA sequences: Figure 7.2). As concluded by Bateman (1999a: 446), if morphological evolution follows a punctuational pattern (dictated by long periods of stabilising selection that are only occasionally broken by temporary release from selection and consequent speciation) and thus there is no morpho- logical clock, but if in contrast genomic mutation is broadly clock-like, then in phylogenetic terms the vast majority of morphological character-state transi- tions occur during speciation events and the vast majority of molecular charac- ter-state transitions occur between them. This important conclusion primarily contrasted morphological phylogenetic data with sequence data for the regions of the plant genome used routinely to infer plant phylogeny, which lack morphological expression. The key morphogenetic genes at the heart of this chapter are also likely to mutate in a broadly clock-like fashion (e.g. Moller and Cronk, 2001) but there the similarity ends. Contrary to the quote from Chase et al. (2000) that began this section, there is no requirement for instanta- neous, well-honed adaptation, nor for the key gene to wait (at least, not for long) for its cohort of attendant genes to follow its evolutionary lead in order to create a novel 'overall genetic environment'. Genetic control of morphogenesis is not a democracy; rather, key characters reflect key transitions in key genes that are capable of autocratically altering the environment of gene expression. Before exploring these concepts further, we will present two case studies to illus- trate the morphological elements that underpin saltation theory. 7.5 Recognising and interpreting terata in extant and extinct species [EJveryone admits that there are at least individual differences in species under nature. But, besides such differences, all naturalists have admitted the existence of varieties, which they think sufficiently distinct to be worthy of record in Saltational evolution 123 systematic works. No one can draw any clear distinction between individual dif- ferences and slight varieties; or between more plainly marked varieties and sub- species, and species. (Jones, 1999: 447) Hereafter we shall be compelled to acknowledge that the only distinction between species and well-marked varieties is that the latter are known, or believed, to be connected at the present day by intermediate gradations, whereas species were formerly thus connected ... It is quite possible that forms now generally acknowledged to be merely varieties may hereafter be thought worthy of specific names. (Jones, 1999:463) Bateman and DiMichele (1994a) used two detailed examples to illustrate saltation. Reticulate saltation (little discussed in this chapter) was exemplified by the phyloge- netic study of the asterid genus Montanoa (Funk and Brooks, 1990), which showed multiple origins of polyploids, each intimately related to similar transitions in ecolo- gical preferences (like many studies initially investigated by morphological ciadistics alone, this interpretation required some revision following the acquisition of sequence data). Dichotomous saltation (the focus of this chapter, as it is mutationally driven) was illustrated using frequent and profound architectural transitions within the largely fossil clade of rhizomorphic lycopsids (Bateman et al., 1992; Bateman, 1994). Although a dominant element in Palaeozoic floras (Phillips and DiMichele, 1992), this clade has left only a single extant genus, Isoetes (including Stylites), which is highly morphologically reduced and ecologically specialised. This paucity of extant descendants renders the clade as a whole immune to both molecular phyiogenetics and comparative evolutionary-developmental genetics. The arguments in favour of a strong evolutionary-developmental underpinning to the remarkable morphological diversification of the clade were therefore of necessity based on indirect, circumstan- tial evidence, which leaves the case unproven, however credible the underlying logic and biological inferences. Here we will briefly review two other case studies that illustrate various aspects of dichotomous saltation: the first is based on a wholly extinct group of Palaeozoic gymnosperms, whereas the second concerns extant terrestrial orchids, particularly those of the subtribe Orchidinae. 7.5. / Palaeozoic /yginopterid pteridosperms: transient loss of gender segregation The earliest seed-bearing plants were the lyginopterid pteridosperms, which prob- ably evolved from a single progymnospermous ancestor in the late Devonian (e.g. Rothwell and Scheckler, 1988). The pattern of morphological character acquisition within the group demonstrates progressive increase in reproductive sophistication (Retallack and Dilcher, 1988; Rothwell and Scheckler, 1988), but there is strong cir- cumstantial evidence that even the earliest pteridosperms segregated male reproduc- tive organs (clusters of increasingly synangial pollen-organs producing proximally 124 R. M. Bateman and W. A. DiMichele germinating pre-poUen) from female reproductive organs (increasingly cupulate clus- ters of increasingly integumented ovules). The most common architectural model shows strong developmental similarity between male and female architectures; both were borne in dichotomously and three-dimensionally branching structures in the forks of complexly branched pinnate fronds. The most complete known specimen of such a plant, Diplopteridium holdenii, bears several fertile fronds, and each frond is uniformly female (Rowe, 1988). Thus, the available evidence strongly suggests that the plants were either dioecious or at best sequentially monoecious, presumably to ensure cross-pollination. The only known exception to this rule is a single barely hermaphrodite specimen of the early Carboniferous lyginopterid ovulate cupule Pullaritheca longii (Long, 1977a, b; Rothwell and Wight, 1989); all other 38 Pullaritheca cupulcs recovered from two small adjacent outcrops in Southeast Scotland are uniformly ovulate (Bateman and Rothwell, 1990). Each cupule ('hemicupulc' sensu Long, 1977a) is a pendulous bowl 7-10 mm long and 5-8 mm in diameter, consisting of six to twelve fleshy finger-like lobes surrounding a central discoid placenta (Figures 7.3a and 7.4a). The placenta bears twenty to thirty ovules that terminate in a characteristic chambered ('hydropteridalean') pollen-receiving apparatus, formed from the nucel- lus and well adapted to accommodate wind-borne pre-pollen grains retracted into the chamber via a pollen-drop mechanism (Figure 7.3b: Rothwell and Scheckler, 1988). The ovules expanded and matured into viable seeds only once they had been pollinated, eventually being shed from the cupule; consequently, most of the ovules remaining in the Pullaritheca cupules are unexpanded and abortive, presumably because they had not been pollinated (Figures 7.3a and 7.4a). The exceptional hermaphrodite cupule was described in detail by Long (1977a), prompting him to indulge in a rare venture into biological speculation. Specifically, it allowed Long (1977b) to resurrect with greater conviction his earlier (Long, 1966) cupule-carpel theory, which suggested that angiosperms could have evolved directly from derived Mesozoic pteridosperms such as Caytonia (e.g. Harris, 1964; Retallack and Dilcher, 1988) by retention of the ovules within fully fused sterile cupules. This ? f Figure 7.3 An example of a fossil putative teratos from the Lower Carboniferous of Oxroad Bay, East Lotliian, Scotland. Longitudinal sections through the margin of an exceptional speci- men of the early seed-fern cupule Pullaritheca longii (Lyginopteridaceae: Pteridospermales), showing a transition from (c) regulated expression of ovules to (a) atavistic expression of microsporangia via (b) non-functional structures of indeterminate gender, (a-c) modified from Long, 1977a, Figure Ic, e, i). Labels: L, left hemisphere; R, right hemisphere; ov, ovule; sm, microsporangium; ch, chimaeric structure possessing features of both ovule and microsporangium. (X4.8: after Bateman and DiMichele, 1994b, Figure 9.) trnf- ^ Figure 7.4 An example of a fossil putative teratos from the Lower Carboniferous of Oxroad Bay (see also Figure 7.3). (a) Portion of one of thirty-eight recorded dehisced specimens of the lobed placental cupule Pullaritheca longii that exclusively bear Hydrasperma longii ovules, showing retention of a few small abortive ovules attached to the vascularised pla- centa, (b-c) Two teratological structures first discovered by Long (1977a) at the margin of a single atypical cupule, suggesting ectopic expression of microsporangia; (b) largely resembles an abortive ovule but has undergone exceptional proliferation of the distal nucellar tissue that is normally adapted for capturing pre-pollen grains; (c) shows similar nucellar proliferation to (b), but contains many poorly-formed microspores rather than the expected single permanently retained megaspore. (d) The typical pollen-receiving chamber of Hydrasperma ovule, compressed by development of the ovum following suc- cessful fertilisation (see also Long, 1977a, b; Rothwell and Wight, 1987; Bateman and Rothwell, 1990; Bateman and DiMichele, 1994b). Magnifications: (a, b, d) x 63, (c) x 125. Photographs by RMB. I 126 R. M. Bateman and W. A. DiMichele theory was dealt an apparently fatal blow by well-known morphological phyloge- netic analyses of the 1980s and 1990s (beginning with Crane, 1985; Doyle and * Donoghue, 1986). These phylogenies consistently resurrected and promoted the *" Anthophyte hypothesis, which interpolated between paraphyletic pteridosperms and monophyletic angiosperms various putatively derived gymnosperms (conifers and their relatives, pentoxylaleans, bennettites, and gnetaleans), rendering impossible the ' direct transition from pteridosperm to angiosperm. However, this conclusion has been seriously challenged by some arguments that revised morphological homologies place the bennettites as sister to the cycads (W. > Crepet, pers. comm. 2001) and, more importantly, recent polygenic phylogenies that placed the gnetophytes as a derived clade within a now monophyletic clade of extant gymnosperms (cf. Mathews and Donoghue, 1999; Qiu et ai, 1999; Chaw et ai, 2000; Frohlich and Parker, 2000; Graham and Olmstead, 2000). This topology was supported by evolutionary-developmental genetic evidence of synapomorphic loss of the Needle copy of Ify from angiosperms (Frohlich, 2001, 2002), prompting the development of the Mostly Male theory of angiosperm origin (Frohlich and Parker, ? 2000; Frohlich, 2001, 2002), which requires the ectopic expression of ovules on for- .? f merly male sporophylls. Does the hermaphrodite Fullaritheca cupule have any bearing on the credibility of these important but highly speculative hypotheses? I 1 The existence of thirty-eight wholly ovulate cupules demonstrates that the one ' recorded hermaphrodite cupule is an exceptional occurrence that has taken place within a routinely unisexual species (in other words, the hermaphrodite ^ cupule is a developmental 'accident'), especially when viewed in the context of .^ the fact that all other Palaeozoic pteridosperms have reliably unisexual repro- ductive clusters. 2 The near-radial symmetry of the cupule contrasts strongly with the localisation " of the sporangia along a small, marginal portion of the placenta (Long, 1977a) (Figure 7.3). More symmetrical segregation of the genders, most probably with the male sporangia distributed along the entire periphery of the placenta, would i be expected from a stable, genetically controlled hermaphrodite cupule. 3 The presence of two phenotypically intermediate structures at the junction of the ovulate and microsporangiate zones of the placenta also casts doubt on the stability of the hermaphrodite phenotype. One of these structures (Figure 7.4b) k largely resembles the abortive Hydrasperma ovules shown in Figure 7.4a, retain- ? ing the tentacle-like distal lobes of the integument that give this ovule-genus its name. However, the nucellus-derived pollen chamber (Figure 7.4d) is absent, being replaced by an asymmetric, 'cancerous' outgrowth of the nucellus. This * nucellar proliferation is also evident in the second structure (Figure 7.4c), which otherwise more closely resembles a microsporangium, even producing within the nucellar envelope a large number of incompletely formed pre-poUen grains. Taken together, these three observations suggest to us that the developmental anomaly is the product of a local physiological perturbation rather than being geneti- cally determined. The two phenotypically 'hybrid' structures imply that there was a h breakdown in gender control across the placenta and that the mechanism of gender ??' control was expressed clinally. This accords with gender control of the unisexual Saltational evolution 127 cones of extant conifers, where nutritional clines separate pollen-bearing cones from the better resourced ovulate cones. In the case of the hermaphrodite Pullaritheca cupule, one possible explanation lies in the apparently relatively poor vasculature supplying the microsporangium-bearing margin of the cupule (R. Bateman, unpubl. obs.). Thus, the cupule is undoubtedly a teratos, reflecting an instantaneous phenotypic shift within an individual, but if the above interpretation is correct, it is not a hona fide hopeful monster (Table 7.1), as the phenotypic shift is not heritable. Nonethe- less, the aberrant cupule provides a useful insight into the control of gender expres- sion in pteridosperms, which in turn suggests that a genuinely genetically controlled mutation could indeed allow ectopic expression of male structures on a fundament- ally female structure to produce a flower precursor. It also suggests the feasibility of the converse phenomenon, namely ectopic expression of female structures on a fundamentally male structure, that is required for the Mostly Male theory (Frohlich, 2002). And lastly, it indicates the potential contribution to plant evolution of heterotopy. Strictly, heterotopy is a spatial shift in a developmental programme and its result- ing phenotypic structure across the bauplan of an organism (cf. Bateman, 1994; Crane and Kenrick, 1997; Frohlich and Parker, 2000; Baum and Donoghue, 2002; Cronk, 2002; Kellogg, 2002; Rudall and Buzgo, 2002). In the utilitarian terminol- ogy of Baum and Donoghue (2002), a shift of a structure to a new location is termed a 'neoheterotopy', whereas the at least partial replacement of a pre-existing structure is a 'homeoheterotopy' (complete replacement of the structure constitutes homeosis s.s.: see also the following section). Given their pivotal position in the phylogeny of seed-plants, it is especially unfor- tunate that there are no extant pteridosperms available to be subjected to the full panoply of evolutionary-developmental genetic techniques. In order to learn more of the evolutionary power of heterotopy, we will now consider a strongly contrast- ing clade that has an exceptionally poor fossil record (e.g. Mehl, 1986) but is remarkably species-rich in the extant flora. 7.5.2 Floral symmetry and speciation in orchids: many attempts yield few successes 7.5.2.1 Background and terminology The literal blossoming of plant evolutionary-developmental genetics was spear- headed by studies of heterotopy sensu lato in relatively derived eudicot angiosperms (notably the model genera Antirrhinum and Arabidopsis), allowing elucidation of the basic ABC model of organ identity (e.g. Coen and Meyerowitz, 1991) that is now becoming far more complex as new data constantly demand revisions and amendments (e.g. Cubas, 2002; Theissen et ah, 2002). It was inevitable that this would soon lead to reconsideration of an old evolutionary chestnut, floral symmetry (e.g. Coen, 1999; Endress, 1999, 2001; Cubas et ai, 2001; Cubas, 2002; Knapp, 2002; Rudall and Bateman, 2002). To classical morphologists the traditional primary distinction in floral symmetry separates 'regular' radial symmetry (actinomorphy) from 'irregular' bilateral symmetry 128 R. M. Bateman and W. A. DiMichele r i ' I (zygomorphy), though this fundamental dichotomy requires amendment to take into account of irregular flowers that lack any recognisable symmetry (asymmetric sensu Endress, 2001; anartiomorphic sensu R. Bateman and L. McCook, unpubl. obs.). Actinomorphy and zygomorphy can be defined largely on recognisable numbers of mirror planes (planes that divide the flower into two mirror images when viewed perpendicular to the pedicel); there are at least two and usually more in actinomor- 'f phy, and typically one in zygomorphy (a few zygomorphic flowers possessing four > mutually perpendicular sepals and/or petals arranged in opposing pairs of unequal j size have two unequal mirror planes: Rudail and Bateman, 2002). Sadly, this well-established botanical terminology has been mutated by develop- mental geneticists to create a tension that is clearly evident in this volume; actin- omorphic flowers have been termed 'symmetrical' and zygomorphic flowers j: 'asymmetrical', prompting Endress (1999, 2001) to redescribe actinomorphic ^ flowers as polysymmetric and zygomorphic flowers as monosymmetric. Here, we \ retain the standard botanical terminology, noting also that (a) with regard to the i vertical axis in zygomorphic flowers the botanical preference for the term 'dors/ven- * tral' is more linguistically correct than the prevalent developmental genetic prefer- ^ f ence for the term 'dorsoventral' (cf. Brown, 1956), and (b) the term dorsoventral has a contrasting meaning in the developmental anatomy of animals (Kaplan, 2001a). J A third complication is that these descriptions of symmetry tend to be used to Ti characterise the whole flower, when the symmetries of each of the four fundamental \ whorls can in theory be different (often, perianth symmetry is prioritised and stamen , and carpel symmetry are essentially ignored: Bateman, 1985). Eor example, the flowers of Antirrhinum are zygomorphic in all four whorls, whereas those of Ara- i" bidopsis appear actinomorphic until one observes the characteristic but subtle bilat- ^ eralism evident in stamen insertion and early sepal development. It is therefore j preferable to consider the symmetry of each of the four whorls separately, rather ;. than attempt to summarise the symmetry of an entire flower in a single aggregate \ term. j 7.5.2.2 A survey of floral terata in terrestrial orchids T* i V Bateman (1985) reviewed occurrences of floral terata among British orchids, focus- ing on examples of peloria: any transition from zygomorphy to actinomorphy or vice versa (see also Eeavitt, 1909; Thei^en, 2000). Noting that the gynostemium (a fusion of the male and female whorls) always retained a degree of bilateralism, he focused on transitions in floral symmetry of the three sepals plus the three petals, taking into account the usual strong morphological differentiation of the median ^ petal. This petal, termed the labellum, acts as a landing stage for pollinating insects in most species; hence, although it is developmentally uppermost, in most cases it is spatially lowermost; in erect inflorescences this is due to a 180? torsion of the ovary that is termed 'resupination' (Ernst and Arditti, 1994; Rudail and Bateman, 2002). Three categories of morphological transition were evident: type A peloria, when the two lateral petals are replaced by two additional labella (cf. Figure 7.5a, b), the less common type B peloria, when the labellum is replaced by an additional lateral petal, and a third category of more heterogeneous morphological transitions that were collectively termed pseudopeloria by Bateman (1985). Here, the modified (a) (c) (b) (d) figure 7.5 Two examples of extant teratos and putative hopeful monsters from the orchid subtribe Orchldinae. (a) is a typical flower of the insect-pollinated orchid Ophrys insectifera from Hampshire, England, that shows complex adaptations for transfer of pollinia via cephalic pseudocopulation by male solitary wasps, (b) is a flower of an adjacent individual showing type A perianthic peloria sensu Bateman (1985); the two mimicked 'antennae' of (a) have been homeotically replaced by additional 'bodies', (c) is a typical flower of Platanthera chlorantha from Perthshire, Scotland, that shows a long, nectariferous spur, fragrance and white coloration adapted to attract night-flying moths as pollinators, (d) is the flower of an adjacent individual showing pseudopeloria sensu Bateman (1985); the petals of the normal flower, including the elaborate labellum and spur, have been replaced by three additional sepal-like structures (see also Figure 10 of Rudall and Bateman, 2002). Magnifi- cations: (a) X 2.5, (b) X 1.9, (c) x 2.9, (d) x 2.6. (a-c) by RMB, (d) courtesy of R. Bush. K 130 R. M. Bateman and W. A. DiMichele labellum becomes less distinctive than the typical labellum but can still be differenti- . ated from the lateral petals and so confers a degree of zygomorphy to the petal ^ whorl (cf. Figure 7.5c, d; Plate la, b). Often, the modified labellum more closely resembles the sepals than either the lateral petals or the normal labellum, and hence it is frequently termed 'sepaloid' in the literature. Similar floral transitions occur in .^ other plant families but are rarely described, perhaps because they are less immedi- 'i ately obvious than genuinely peloric morphs. Adding a fourth (and rarer) phenome- [ non to the classification of Bateman, Horsman (1990) recognised type C peloria, ; wherein all three petals are apparently replaced by sepals, generating two near-iden- i^ tical whorls of three perianth segments (see also Lang, 2001). j" Given the above definitions, one might interpret both type A and type B peloria in , orchids as lateral homeoheterotopy (i.e. a change of organ identity confined to a ; single whorl, namely the three petals) and type C peloria and pseudopeloria as vertical homeoheterotopy (a change of organ identity between two whorls; in this case, apparent expression of three sepals and one sepal respectively in the relatively acropetal petal whorl). However, in most cases of pseudopeloria it is also possible to view the 'sepaloid' labellum as reflecting one or more changes in the timing of devel- opment {heterochrony); specifically, its simplicity relative to the typical labellum could in theory reflect a labellum whose development had either slowed (neotenic) or ceased abnormally early (progenetic) to yield a mature structure that resembles the juvenile stage of the homologous structure in a notional ancestral organism (pae- domorphic: all terminology pertaining to heterochrony follows Alberch et al., 1979; see also McKinney and McNamara, 1991; Zelditch and Fink, 1996). Systematic and causal interpretation of such terata depends strongly on the level of comparison of the 'homeotic' (s./.) morph with the normal 'wild type' morph. In the most obvious case, bimodal variation in floral symmetry within a single indi- vidual (e.g. Darwin, 1859; analogous to the hermaphroditic Pullaritheca cupule described above) is likely to reflect a non-genetic cause or a somatic mutation, and thus be of no evolutionary potential. Nonetheless, interpretation is simplified by the fact that the conspecificity of both morphs is assured, and the identity of the abnor- mal morph can therefore be determined by comparison with other conspecific indi- viduals bearing only one floral morph. Examples occur widely within the orchid family; the most common manifestation is the duplication of the labellum to produce a perianth of seven segments, a phenomenon that typically affects only the lowermost or the uppermost flowers of a (usually unbranched) orchid inflorescence. Determining the conspecificity of the homeotic and normal floral morphs becomes more challenging when they are borne on separate individuals. In most cases, both morphs co-exist in a single local population, and resemble each other in all other phe- notypic characters. However, distinguishing the normal morph from the homeotic morph (i.e. determining the polarity of the morphological transition) can be challeng- ing, usually relying on the homeotic morph being appreciably less frequent than the normal morph in the populations within which it occurs or, even less convincingly, in its absence from other closely related species. This was the case with the type A peloric individual of Ophrys insectifera shown in Figure 7.5b, which was the only such morph observed in an estimated population of 6,000 flowering plants. However, this assumption of relative rarity is not always justified, especially in popu- lations of orchid species that are autogamous; for example, Epipactis phyllantbes var. Saltational evolution 131 phyllanthes (Young, 1952; Bateman, 1985) often forms uniformly pseudopeloric populations, presumably because their self-pollination leads to very low genetic diver- sity (Hollingsworth et al., subm.). Under such circumstances, arguments for transi- tional polarity generally rely on the existence of many populations that wholly lack the putatively homeotic morph (as is the case for E. phyllanthes s.L: Young, 1952). In such cases, the homeotic morph is likely to reflect a mutation (or combination of mutations) that is by definition polymorphic within the populations under scrutiny. More usefully, previous unsubstantiated assertions of conspecificity or lack of conspecificity between the two contrasting floral morphs can now be readily tested using molecular markers. For example, a wide range of markers failed to detect any differences between normal and pseudopeloric E. phyllanthes (P. Hollingsworth, R. Bateman et al., unpubl. obs.). Molecular data are especially valuable for refuting previous accusations of hybrid origins for homeotic (especially pseudopeloric) morphs. McKean (1982) interpreted the orchid shown in Figure 7.5d as a bigeneric hybrid between Platanthera chlorantha and Pseudorchis albida, whereas Bateman (1985) argued that it was probably a pseudopeloric morph of P. chlorantha (Figure 7.5c). This species is frequent at the locality yielding the supposed hybrid, where the vegetation includes several teratologies that are thought to reflect the high heavy metal content of the underlying spoil heaps. Nuclear rDNA (ITS) sequences revealed a large phylogenetic disparity between Platanthera and Pseudorchis (Bateman et al., 1997; Pridgeon et al., 1997; Bateman, 1999a, 2001) and further studies using mole- cular markers have conclusively demonstrated that the contrasting plants shown in Figure 7.5c and d are, in fact, both assignable to P. chlorantha. Homeosis becomes of greatest interest to systematists when the putative homeotic morph regularly forms fairly uniform populations and hence becomes recognised as a distinct taxonomic species (cf. Bateman and DiMichele, 1994a; Rudall and Bateman, 2002). In other words, the teratology in question definitely reflects muta- tion, and that mutation has become fixed in the populations in question. Under these circumstances, we can usefully apply the full panoply of morphological and molecular phylogenetic techniques to the problem. In some such cases the mutant orchid species is assigned to a pre-existing genus, a good example being the type B peloric cypripedioid Phragmipedium lindenii (e.g. Pridgeon et al., 1999). In other cases, particularly in the Orient, the florally simpli- fied mutant has been controversially recognised not only as a distinct species but also as a monotypic genus that is assumed to be phylogenetically primitive. Of these supposed genera (most of which are lower epidendroids: for reviews see Chen, 1982; Rudall and Bateman, 2002), Tangtsinia closely resembles Cephalanthera, Sinorchis appears attributable to either Cephalanthera or, more likely, Aphyllorchis, and Dip- landrorchis and the polyspecific Archineottia resemble Neottia. Within the orchi- doids, Aceratorchis is a more widely distributed hona fide species that resembles the co-occurring genus Galearis. Rudall and Bateman (2002) suggested that, far from being primitive, DNA sequence data will demonstrate that these 'genera' are nested within other more species-rich genera that possess much more strongly differentiated labella. Available data are insufficient to determine whether the morphs show types B or C peloria or pseudopeloria. A similar example is evident among South African orchidoids of the Satyrium group, where two 'subactinomorphic' (pseudopeloric) species possessing reduced 132 R. M. Bateman and W. A. DiMichele labella and elongate gynostemia have been assigned to the genus Pachites. It is not clear whether these two species are sisters, nor whether they are the sister group, and potentially ancestral to, Satyrium s.s. or nested within Satyrium as secondarily reduced morphs (Linder and Kurzweil, 1999). Although molecular phylogenies have begun to be constructed for South African orchids (Douzery et ai, 1999; Bateman et al., subm.), this putative genus has not yet been sequenced. 7.5.2.3 Possible post-saltational radiations In yet other cases, the prospecies not only successfully estabhshes a new taxonomic species and genus but also subsequently radiates to generate several descendant species, often via polyploidy and/or a transition from allogamy to autogamy. The type B or C peloric genus from Australasia, Thelymitra, has been demonstrated using sequence data to be monophyletic (Kores et al., 2001) and contains c. fifty species, many of which are autogamous (Bower, 2001; Bateman and Rudall, 2002). Here, however, we have chosen to focus on the pseudopeloric European genus Nigritella, as we have access to both molecular and morphological phylogenetic data and so can conduct a cross-matrix comparison (Figure 7.6: cf. Bateman, 1999a). Nigritella contains about fifteen species, most reflecting relatively recent polyploidy events and/or transitions from allogamy to autogamy (Hedren et al., 2000). ITS sequence data (Figure 7.6b) imply that Nigritella is nested phylogenetically within a paraphyletic Gymnadenia s.s. (consequently, Nigritella was sunk into Gymnadenia by Bateman et al., 1997), and that both putative genera are appreciably divergent from their sister genus, Dactylorhiza. The morphological cladistic analysis (Figure 7.6a) similarly suggests that Nigritella is nested within Gymnadenia, but identifies a contrasting sister-species. More interestingly, it also reveals that the equal longest morphological branch in the tree separates Gymnadenia s.s. from Nigritella. Although the two putative genera are very similar vegetatively, Gymnadenia s.s. has far more strongly zygomorphic and fully resupinate flowers that possess long nectar- iferous spurs and are pollinated by lepidoptera (Figure 7.7a-c). In contrast, Nigritella lacks resupination and has only a simplified labellum and vestigial spur (Figure 7.7d-f); these are classic characteristics of pseudopeloria (Bateman et al., 1997, subm.; Pridgeon et ai, 1997; Bateman, 1999a, 2001; Rudall and Bateman, 2002). Interestingly, there is no measurable sequence divergence or qualitative morpho- logical divergence among the several (arguably over-split) species of Nigritella, prompting Bateman (1999a) to suggest that the radiation of this group, which is confined to alpine and boreal habitats in Europe, may reflect a species-level radia- tion that occurred since the Pleistocene ice retreated at the close of the Loch Lomond Stadial (Younger Dryas), about 10,000 years ago. However, as noted by M. Frohlich (pers. comm. 2001), the present distributions could be the relicts of a genus that was more widespread during the Pleistocene glacials, when terrains suit- able for the plants would have been more extensive. In either case, much of the driving force for that radiation appears to have been polyploidy and at least one transition to autogamy, suggesting that the clade is 'attempting' to maximise its fitness within the 'undesirable' constraint of a floral morphology that can no longer support the ancestral lepidopteran pollination syndrome. It is regrettable that greater progress has not been made in the evolutionary-developmental genetics of Saltational evolution 133 (a) morphology c Platanthera bifolia (OG2) Pseudorchis albida s.s. (OGI) Dactylorhiza (Coelogl.) viridis Dactylorhiza euxina Dactylorhiza incarnata Gymnadenia conopsea s.s.* Gymnadenia orchidis Gymnadenia borealis Gymnadenia densiflora ?Nigritella' nigra s.s. 'Nigriteila' austriaca 'Nigritella' miniata (rubra) Gymnadenia odoratissima Gymnadenia conopsea s.s.* (b) ITS sequences 1 V 30 steps 3 10 steps figure 7 6 Comparison of one of two most-parsimonious cladograms for morphology (a) and one of several most-parsimonious cladograms for ITS sequences (b) for the GYwnaden.a alliance (boldface), its sister-group the Daaylorhiza alliance, and Pseudorchis plus Platanthera as a paraphyletic outgroup (all Orchidinae: Orchidaceae). Branch lengths are proportional to the number of steps under Acctran optimisation. Cross-bars indicate unambiguous inde^; nodes bearing question marks have less than 80 per cent bootstrap support. Note the incongruent positions betv^een the two trees of Gymnadenia conopsea s.s (asterislC Francis, London, pp. 206-219. V Jones, J. S. (1 999). Almost Like a Whale: the Origin of Species Updated. Doubleday, London. Kaplan, D. R. (2001a) Fundamental concepts of leaf morphology and morphogenesis: a con- tribution to the interpretation of molecular genetic mutants. International journal of Plant Sciences, \61, 46.5-474. Kaplan, D. R. (2001b) The science of plant morphology: definition, history, and role in modern biology. American journal of Botany, 88, 1711-1741. Kauffman, S. A. (1993) The Origins of Order: Self-Organization and Selection in Evolution. Oxford University Press, Oxford. Kellogg, E. A. (2002) Are macroevolution and microevolution qualitatively different? Evidence from Poaceae and other families, in Developmental Genetics and Plant Evolution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 70-84. Kenrick, P. (1994) Alternation of generations in land plants: new phylogcnetic and palaeob- otanical evidence. Biological Reviews, 69, 293-330. Kenrick, P. (2002) The Telome Theory, in Developmental Genetics and Plant E,volution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 365-387. Kenrick, P. and Oanc, P. R. (1997) The Origin and Early Diversification of Plants on Land: A Cladistic Study. Smithsonian Institution Press, Washington, DC. Kimura, M. (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press. Kimura, M. (1991) Recent development of the neutral theory viewed from the Wrightian tra- dition of theoretical population genetics. Proceedings of the National Academy of Sciences of the USA, 88, 5969-5973. Knapp, S. (2002) Floral diversity and evolution in the Solanaceae, in Developmental Genetics and Plant Evolution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 267-297. Kores, P. J., Molvray, M., Weston, P. H., Hopper, S. D., Brown, A. P., Cameron, K. C. and Chase, M. C. (2001) A phylogcnetic analysis of Duiridcac (Orchidaceae) based on plastid DNA sequence data. American Journal of Botany, 88, 1903-1914. Kramer, E. M. and Irish, V. F. (1999) Evolution of genetic mechanisms controlling petal development. Nature, 399, 144-148. Kramer, E. M. and Irish, V. F. (2000) Evolution of the petal and stamen developmental pro- grams: evidence from comparative studies of the lower cudocts and basal angiospcrms. International Journal of Plant Sciences, 161, S29-S40. Kuhn, T. S. (1962) The Structure of Scientific Revolutions. Chicago University Press, Chicago. ' f Saltational evolution 155 I.andc, R. (1986) The dynamics of peak shifts and the pattern of morphological evolution. Faleobiology, 12, 343-354. Landwchr, j. (1977) Wilde Orchideeen Van Europa. Amsterdam. Lang, D. C. (2001) A new variant of Ophrys apifera in Britain. BSBl News, 88, 40-46. Langdale, j. A., Scotland, R. W. and Corley, S. B. (2002) A developmental perspective on the evolution of leaves, in Developmental Genetics and Plant Evolution (eds Q. C. B. Oonk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 388-394. Lauder, G. V. (1990) Functional morphology and systematics: studying functional patterns in a historical context. Annual Revieiv of Ecology and Systematics, 21, 317-340. Lcavitt, R. G. (1909) A vegetative mutant, and the principle of homeosis in plants. Botanical Gazette, 47, 30-68. Levin, D. A. (1970) Developmental instability and evolution in peripheral isolates. Evolution, 104, 343-353. Levin, D. A. (1993) Local speciation in plants: the rule not the exception. Systematic Botany, 18, 197-208. Levin, D. A. (2000) The Origin, Expansion, and Demise of Plant Species. Oxford University Press, Oxford. Levin, D. A. (2001) Fifty years of plant speciation. Taxon, 50, 69-91. Levinton, J. (1988) Genetics, Paleontology, and Macroevolution. Cambridge University Press, Cambridge. Lewis, H. (1962) Catastrophic selection as a factor in speciation. Evolution, 16, 257-271. Lewis, H. (1966) Speciation in flowering plants. Science, 152, 167-172. Lewis, H. (1969) Speciation. Taxon, 18, 21-25. Linder, H. P. and Kurzweil, H. (1999) Orchids of Southern Africa. Balkema, Rotterdam. Long, A. G. (1966) Some Lower Carboniferous fructifications from Berwickshire, together with a theoretical account of the evolution of ovules, cupules and carpels. Transactions of the Royal Society of Edinburgh B, 66, 34.5-375. Long, A. G. (1977a) Some Lower Carboniferous pteridosperm cupules bearing ovules and microsporangia. Transactions of the Royal Society of Edinburgh B, 70, 1-11. Long, A. G. (1977b) Lower Carboniferous pteridosperm cupules and the origin of the angiosperms. Transactions of the Royal Society of Edinburgh B, 70, 13-35. Luo, D., Carpenter, R., Copsey, L., Vincent, C, Clark, J. and Coen, E. (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell, 99, 367-376. McKcan, D. R. (1982) X Pseudanthera breadalbanensis McKean: a new integeneric hybrid from Scotland. Watsonia, 14, 129-131. McKinney, M. L. and McNamara, K. J. (1991) Heterochrony: The Evolution of Ontogeny. Plenum, New York. Mcl.ellan, T., Shephard, H. L. and Ainsworth, C. (2002) Identification of genes involved in evolutionary diversification of leaf morphology, in Developmental Genetics and Plant Evo- lution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor &: Francis, London, pp. 315-329. McVean, G. T. and Hurst, L. T. (1997) Evidence for a selectively favourable reduction in the mutation rate of the X chromosome. Nature, 386, 388-392. Maddison, W. P. (1990) A method for testing the correlated evolution of two binary charac- ters: are gains or losses concentrated on certain branches of a phylogenetic tree? Evolution, 44, 539-557. Mallet, J. and Joron, M. (1999) Evolution of diversity and warning colour and mimicry: poly- morphisms, shifting balance, and speciation. Annual Revieiv of Ecology and Systematics, 30, 201-233. Margulis, L. (1993). Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons (2nd edn). Freeman, New York. 156 R. M. Bateman and W. A. DiMichele Marshall, C. R., Orr, H. A. and Patel, N. H. (1999) Morphology innovation and develop- ? mental genetics. Proceedings of the National Academy of Sciences of the U.S.A., 96, 9995-9996. Martin, W. and Schnarrenberger, C. (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Current Genetics, 32, 1-18. ,, Mathews, S. and Donoghue, M. J. (1999) The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science, 282, 947-950. Maynard Smith, J. (1989) Evolutionary Genetics. Oxford University Press, Oxford. * Maynard Smith, J. and Szathmary, E. (1995) The Major Transitions of Evolution. Freeman, Oxford. Mayr, E. (196,3) Animal Species and Evolution. Belknap Press, Harvard. Mehl, J. (1986) Die fossile Dokumentation der Orchideen. Journal Berlin Naturwis- ? senschaften Verein Wuppertal, 39, 121-133. v Meyerowitz, E. M. and Somerville, C. R. (1994) Arabidopsis. Cold Spring Harbor Labora- tory Press, New York. Mindell, D. P. and Meyer, A. (2001) Homology evolving. Trends in Ecology and Evolution, v 16,434-440. MoUer, M. and Cronk, Q. C. B. (2001) Evolution of morphological novelty: a phylogenetic analysis of growth patterns in Streptocarpus (Gesncriaceae). Evolution, 55, 91 8-929. \ Morris, R. (2001) The Evolutionists: The Struggle for Darwin's Soul. Freeman, San Francisco. * Nickrent, D. I.., Duff, R. J., Colwell, A. E., Wolfe, A. D., Young, N. D., Steiner, K. E. and * dePamphilis, C. W. (1998) Molecular phylogenetic and evolutionary studies of parasitic i plants, in Molecular Systematics of Plants 2 (eds D. E. Soltis, P. S. Soltis and J. J. Doyle), Chapman &c Hall, London, pp. 211-241. ' Ohta, T. (1992) The nearly neutral theory of molecular evolution. Annual Review of Ecology '' and Systematics, 23, 263-286. Ohta, T. (1995) Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. Journal of Molecular F.volution, 40, 56-63. ^ Orr, H. A. (1991) Is single gene speciation possible? Evolution, 45, 764-769. ^ Orr, H. A. (1998) The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution, 52, 935-949. , Palopoli, M. F. and Patel, N. H. (1998) Evolution of the interaction between Hox genes and a downstream target. Current Biology, 8, 587-590. Patterson, C. (1999) Evolution (2nd edn). Natural History Museum, London. Phillips, T. L. and DiMichele, W. A. (1992) Comparative ecology and life-history biology of arborescent lycopsids in Late Carboniferous swamps of Euramerica. Annals of the Mis- ' souri Botanical Garden, 79, 560-588. Poethig, R. S. (1990) Phase change and the regulation of shoot morphologies in plants. Science, 250, 923-930. Pomiankowski, A. and Hurst, L. D. (1993) Siberian mice upset Mendel. Nature, 363, 396-397. Prescott, D. M. and DuBois, M. L. (1996) The mercurial germ-line genome of hypotrichous ciliates, in Genomes of Plants and Animals (eds J. P. Gustafson and R. B. Flavell), Plenum, ^ New York, pp. 271-279. Price, T., Turelli, M. and Slatkin, M. (1993) Peak shifts produced by correlated response to selection. Evolution, 47, 280-290. Pridgeon, A. M., Bateman, R. M., Cox, A. V., Hapeman, J. R. and Chase, M. W. (1997) Phy- ? logcnctics of subtribc Orchidinae (Orchidoideae, Orchidaceae) based on nuclear ITS ' ,_^ sequences. 1. Intergeneric relationships and polyphyly of Orchis sensu lato. Lindleyana, 12,89-109. Saltational evolution 157 Pridgeon, A. M., Cribb, P. J., Chase, M. W. and Rasmussen, F. N. (eds) (1999) Genera Orchidacearum. 1. General introduction, Apostasioideae, Cypripedioideae. Oxford Uni- versity Press, Oxford. Pryer, K. M., Schneider, H., Smith, A. R., Cranfill, R., Wolf, P. G., Hunt, J. S. and Sipes, S. D. (2000) Horsetails and ferns are a monophyletic group and the closest living relatives of seed plants. Nature, 409, 618-622. Qiu, Y.-L., Lee, J., Bernasconi-Quadroni, F., Soltis, D. E., Soltis, P. S., Zanis, M., Zimmer, E. A., Chen, Z.-D., Savolaincn, V. and Chase, M. W. (1999) The earliest angiosperms: evid- ence from mitochondria], plastid and nuclear genomes. Nature, 402, 404^07. Raff, R. A. and Kauffman, T. C. (1983) Embryos, Genes, and Evolution. Macmillan, New York. Retallack, G. J. and Dilcher, D. L. (1988) Reconstructions of selected seed ferns. Annals of the Missouri Botanical Garden, 75, 1010-1057. Richardson, J. E., Pcnnington, R. T., Pennington, T. D. and Hollingsworth, P. M. (2001a) Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science, 293, 2242-2245. Richardson, J. E., Weitz, F. M., Fay, M. F., Cronk, Q. C. B., Linder, H. P., Reeves, G. and Chase, M. W. (2001b) Rapid and recent origin of species richness in the Cape flora of South Africa. Nature, 412, 181-183. Ridley, M. (1996) Evolution (2nd edn). Blackwell, Oxford. Riedl, R. (1979) Order in Living Organisms. Wiley, New York. Riescberg, L. H. (1997) Hybrid origins of plant species. Annual Review of Ecology and Sys- tematics, 28, 359-389. Rieseberg, L. H. and Burke, J. M. (2001) The biological reality of species: gene flow, selec- tion, and collective evolution. Taxon, 50, 47-67. Rieseberg, L. H., Van Fossen, C. and Desrochers, A. M. (1995) Hybrid speciation accompan- ied by genomic reorganisation in wild sunflowers. Nature, 375, 313-316. Rosenzwcig, M. L. and McCord, R. D. (1991) Incumbent replacement: evidence for long-term evolutionary progress. Paleohiology, 17, 202-213. Rothwell, G. W. and Scheckler, S. E. (1988) Biology of ancestral gymnosperms, in Origin and Evolution of Gymnosperms (cd. C. B. Beck), Columbia University Press, New York, pp. 85-134. Rothwell, G. W. and Wight, D. C. (1989) Pullaritheca longii gen. nov. and Kerryia mattenii gen. et spec, nov.. Lower Carboniferous cupules with ovules of the Hydrasperma tenuis type. Review of I'alaeobotany and Palynology, 60, 295-309. Rowe, N. P. (1988) New observations on the Lower Carboniferous pteridosperm Diplo- pteridium Walton and an associated synangiate organ. Botanical Journal of the Linnean Sodery, 97, 125-158. Rudall, P. J. and Bateman, R. M. (2002) Roles of synorganisation, zygomorphy and hetero- topy in floral evolution: the gynostemium and labellum of orchids and other lilioid mono- cots. Biological Reviews. Rudall, P. J. and Buzgo, M. (2002) Evolutionary history of the monocot leaf, in Develop- mental Genetics and Plant Evolution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, pp. 431-458. Rutishauser, R. (1995) Developmental patterns of leaves in Podostemaceae compared with more typical flowering plants: saltational evolution and fuzzy morphology. Canadian journal of Botany, 73, 1305-1317. Sanderson, M. J. (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution, 14, 1218-1231. Sanderson, M. j. (1998) Reappraising adaptive radiation. American Journal of Botany, 85, 1650-1655. Schneider, H., Pryer, K. M., Cranfill, R., Smith A. R. and Wolf, P. G. (2002) Evolution of W8 R. M. Bateman and W. A. DiMichele vascular plant body plans: a!.phyk)genetic perspective, in Developmental Genetics and '^ Plant Evolution (eds Q. C. BJ Cronk, R. M. Bateman and J. A. Hawkins), Tayi'or & Francis, London, pp. 330-364.1 .-? ? ? '? Shapiro, J. A. (1997) Genome organization, natural genetic engineering, and adapti^^e muta- tion; Tre?(is t? Gewei/cs, 13, 98-'li04'.''> . . : ? Shapiro, J. A. (2002) A'21st Centiiriy viewqf evolution^/oMr?a/o/^Bjo/og/<:a/P/;ys/cs (in press). Shubin, N. H.-.and Marshall, C. R. ^^2000) Fossils, genes,'and the origins of novelty. Paleo- biology, 26, 324-340. .''i Z^' . ?. Silvertown, J., Franco,'M.. and Harper,- J.'L. (eds) (1997) 'Plant Life Histories:^ Ecology, ^ Phytogeny and Euolutioni Cambridge University Press, Cambridge. . ' ^ Singh, R. S. and. KHmbas, G..B. (eds) (2000) Evolutionary Genetics: From Molecules to Mor- phology. CarnhndgtUnvversity Psam, Cambridge, i: ; Slack, J. M. W.,^HDllaiid, P. W. H.ahd.Graham, G. F. (1993) The zootype and the phylotypic i stage. Nature, 361,490-492. (.;.!;?- o .i ^ Slatkin, M. (1996):ln kiefense of.foundar-flush theories of speciation. American Naturalist, 147,493-505. ' . / j Stace,' C. A. (1989):P/j?? Taxonomy'.and Bios'ystematics {2nd edn): Arnold, London. 4 Stace, C. A. (1993) The importance ofirarcicvents in ipolyploid ?evolution, in E:volutionary[Patterns and Processes (eds D. R. Lees and D. Edwards), Academic Press, New York, pp.T59:-169. Stebbins, G. L. (1971) CKrgmosomaUEMohition in HigherlPiants. Arno\d,Lond&'n. | Stebbins, G.'Ls',^1983)'Ma'Saic'evwdiowon: an. integrating principle for the modern synthesis. V Experientia, 39, 8234834. r -;r:3-.-,d -.,. ''i , . ? ? ? . ? i . . \ ?.. -i Stein, W. E. (1998) Developmental logic: establishing a relationship betweeaidevelopmehtal ', oprocess and phylogenetic pattern'iirpDifhitive vasculantpknts. Review of'Palaeohot'any and I Pa/y?o/o^y, 102, 15-42. .?'-.-??^ '-.?"'? ? '?..h.nr- -.x'?? \ Templcton, A. R. (1982). Genetic archiftcfiire'of.Speerattonv in Mechanisms of Speciation' (td. '? 1 ?G'..Barigozzi),.Liss, New York,.ppLLl05-121'.>.. "i~ i', ji;.v ? ;. ' i'.s ? IA/O' j Templeton, A. R. (1989) The meaning of. Species'and-spec5ixition:., a'genetic ^perspefcfiwe, in i Speciation and its Consequencesi(tAi^. 0\Kecand cJ.'A. Endle'r), Sinauer, Sijnderland:, MA, V^ pp. 3?27. V.'. ? , .ya.-'^' .'. '< 'a : li ? :* ? ;: ?'' ?... :' >i '".i'-- V.C Teotonio, H. and Rose, M. R. (2001) Reverse evolution (Perspective)'. Evolution, 55, 653-r660. I TheiKen, G.! (2000) Evolutionary; devalcipmental genetics of floral! symmetry: the Revealing power of Linnaeus'monstrous flower!. B/crEssajiSj 22, 2Q9-1-213. ' '.. 'f-^ ? o. i:, ^^ TheiEen,' G.,:Becker, A., Winter, K'.-U.v-Miinfiter; Tif.Kifchncr, C. ;aW Saedler^'. H...(2fiG2-) ( How the land plants learned thetri floiEal AJBGsi.ihe role of.MADSVbox genes an the'evolu- j rionary origin of flowers, .in D/evelopfirent-al 'Genetics^ahd Plant Evolution, (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor & Francis, London, ppi 173-205. ^ TheiKen, G., Kim, J. T. and, Saedleri.;H;:^1996i):;iC^assific?^Hbn land phyloge^iy of the MADS- box gene subfamilies in the morpKdfogiGal je\!i)lutioai'of eukaryotes.i'/owrMa/ of Malecklar Evolution, \0, 4^4^5X6. ? ?,'.?? ; : ? . ? f Saltational evolution 159 Tucker, S. C. (2001) The ontogenetic basis for missing petals in Crudia (Leguminosae: Cae- salpinioideae: Detarieae). International Journal of Pla7it Science, 162, 83-89. Valentine, J. W. (1980) Determinants of diversity in higher taxonomic categories. Paleobiol- ogy, 6, 444-450. Valentine, J. W., Jablonski, D. and Erwin, D. H. (1999) Fossils, molecules, and embryos: new perspectives on the Cambrian explosion. Development, 126, 851-859. Van Steenis, C. G. G. J. (1976) Autonomous evolution in plants: differences in plant and animal evolution. Gardens' Bulletin, Singapore, 29, 103-126. Vermeij, G. J. (1987) Evolution and Escalation. Princeton University Press, NJ. Vogel, J. C., Barrett, J. A., Rumsey, F. J. and Gibby, M. (1999) Identifying multiple origins in polyploid homosporous pteridophytes, in Molecular Systematics and Plant Evolution (eds P. M. Hollingsworth, R. M. Bateman and R. J. Gornall), Taylor & Francis, London. Waddington, C. H. (1957) The Strategy of the Genes. Allen & Unwin, London. Wade, M. J. (1992) Sewall Wright: gene interaction and the shifting balance theory, in Oxford Surveys in Evolutionary Biology 8 (eds D. Futuyma and J. Antonovics), Oxford University Press, Oxford, pp. 35-62. Wade, M. J. and Goodnight, C. J. (1998) The theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments (Perspective). Evolution, 52, 1537-1553. Walbot, V. (2000) A green chapter in the book of life. Nature, 408, 794-795. Walbot, V. (2002) Impact of transposons on plant genomes, in Developmental Genetics and Plant Evolution (eds Q. C. B. Cronk, R. M. Bateman and J. A. Hawkins), Taylor &c Francis, London, pp. 15-31. Wang, R.-L., Stec, A., Hey, A., Lukens, L. and Doebley, J. (1999) The limits of selection during maize domestication. Nature, 398, 236-239. Wendel, J. F., Schnabel, A. and Seelanan, T. (1995) Bidirectional interlocus concerted evolu- tion following allopolyploid speciation in cotton (Gossypium). Proceedings of the National Academy of Sciences of the USA, 92, 280-284. Wessler, S. R., Bureau, T. E. and White, S. E. (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Current Opinion on Genetics and Development, 5, 814-821. Whitlock, M. C. (1997) Founder effects and peak shifts without genetic drift: adaptive peak shifts occur easily when environments fluctuate slightly. Evolution, 51, 1044-1048. Whitlock, M. C., Phillips, P. C, Moore, F. B.-G. and Tonsor, S. J. (1995) Multiple fitness peaks and epistasis. Annual Review of Ecology and Systematics, 26, 601-629. Williams, G. C. (1992) Natural Selection: Domains, Levels and Challenges. Oxford Univer- sity Press, Oxford. Wing, S. L. and Boucher, L. (1998) Ecological aspects of Cretaceous plant radiation. Annual Review of Earth and Planetary Sciences, 26, 379^21. Wolf, J. B., Brodie, E. D. Ill and Wade, M. J. (eds) (2000) Epistasis and the Evolutionary Process. Oxford University Press, Oxford. Wolfe, K. H. (2001) Yesterday's polyploids and the mystery of diploidization. Nature Reviews, Genetics, 2, 333-341. Wray, G. A. (1995) Punctuated evolution of embryos. Science, 267, 1115-1116. Wright, S. (1932) The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the Sixth International Congress of Genetics, 1, 356-366. Wright, S. (1968) Evolution and the Genetics of Populations. Chicago University Press, Chicago. Young, D. P. (1952) Studies in the British Epipactis, III, IV. Watsonia, 2, 253-276. Zelditch, M. L. and Fink, W. L. (1996) Heterochrony and heterotopy: stability and innova- tion in the evolution of form. Paleobiology, 22, 247-250.