Richard M. Bateman

Molecular Systematics and Plant Evolution

1. Using Organelle Markers to Elucidate the History, Ecology and Evolution of Plant Populations R.A. Ennos, W.T. Sinclair, X.-S. Hu and A. Langdon 2. Isolation Within Species and the History of Glacial Refugia C. Ferris, R.A King and G.M. Hewitt 3. The Use of Uniparentally Inherited Simple Sequence Repeat Markers in Plant Population Studies and Systematics J. Provan, N. Soranzo, N.J. McNicol, M. Morgante and W. Powell 4. The Use of RAPD Data in the Analysis of Population Genetic Structure: Case-studies of Alkanna (Boraginaceae) and Plantago (Plantaginaceae) K. Wolff and M. Morgan-Richards 5. Metapopulation Dynamics and Maring-system Evolution in Plants S.C.H. Barrett, J.R. Pannell 6. Identifying Multiple Origins in Polyploid Homosporous Pteridophytes J.C. Vogel, J.A. Barrett, F.J. Rumsey and M. Gibby 7. Population Genetic Structure in Agamospermous Plants R.J. Gornall 8. Monophyly, Populations and Species J.I. Davis 9. Reticulate Evolution in the Mediterranean Species Complex of Senecio Sect. Senecio: Uniting Phylogenetic and Population-level Approaches H.P. Comes and R.J. Abbott 10. The Value of Genomic In Situ Hybridization (GISH) in Plant Taxonomic and Evolutionary Studies C.A. Stace and J.P. Bailey 11. RAPDs in Systematics - a Useful Methodology? S.A. Harris 12. Nuclear Protein-coding Genes in Phylogeny Reconstruction and Homology Assessment: Some Examples From Leguminosae J.J. Doyle and J.L. Doyle 13. Spectral Analysis - a Brief Introduction M.A. Charleston and R.D.M. Page 14. Ribosomal DNA Sequences and Angiosperm Systematics M.A. Hershkovitz, E.A. Zimmer and W.J. Hahn 15. Proteins Encoded in Sequenced Chloroplast Genomes: an Overview of Gene Content, Phylogenetic Information and Endosymbiotic Transfer to the Nucleus B. Stoebe, S. Hansmann, V. Goremykin, K.V. Kowallik and W. Martin 16. Phylogenetics and Diversification in Pelargonium F.T. Bakker, A. Culham and M. Gibby 17. Integrating Molecular Phylogenies and Developmental Genetics: a Gesneriaceae Case Study M. Moller, M. Clokie, P. Cubas and Q.C.B. Cronk 18. Inferior Ovaries and Angiosperm Diversification M.H.G. Gustafasson and V.A. Albert 19. Intergrating Molecular and Morphological Evidence of Evolutionary Radiations R.M. Bateman Albert, The New York Botanical Garden, UK, J.P. Bailey, University of Leicester, UK, F.T. Bakker, University of Reading, UK, J.A. Barrett, University of Cambridge, UK, S.C.H. Barrett, University of Toronto, UK, R.M. Bateman, Royal Botanic Garden, Edinburgh, UK, M.A. Charleston, University of Oxford, UK, M. Clokie, University of Leicester, UK, H.P. Comes, Institut fur Spezielle Botanik und Botanisher Garten, Germany, Q.C.B. Cronk, University of Edinburgh, UK, P. Cubas, Institut Nacional de Investigaciones Agrarias, Spain, A. Culham, University of Reading, UK, J.I. Davis, Cornell University, USA, J.J. Doyle, Cornell University, USA, J.L. Doyle, Cornell University, USA, R.A. Ennos, University of Edinburgh, UK, C. Ferris, University of Leicester, UK, M. Gibby, The Natural History Museum, UK, V. Goremykin, Hans-Knoll-Institut fur Naturstoff-Forschung, Germany, R.J. Gornall, University of Leicester, UK, M.H.G. Gustafsson, The New York Botanical Garden, USA, W.J. Hahn, Columbia University, USA, S. Hansmann, Technische Universitat Braunschwieg, Germany, S.A. Harris, University of Oxford, UK, M.A. Hershovitz, Laboratory of Molecular Systematics, UK, G.M. Hewitt, University of East Anglia, UK, X-S. Hu, University of Edinburgh, UK, R.A. King, University of Leicester, UK, K.V. Kowallik, Heinrich-Heine-Universitat Dusseldorf, Germany, A. Langdon, University of Edinburgh, UK, W. Martin, Technische Universitat Braunschwieg, Germany, J.W. McNicol, Scottish Crop Research Institute, UK, M. Moller, Royal Botanic Gardens Edinburgh, UK, M. Morgan-Richards, Otago University, New Zealand, M. Morgante, Universita di Udine, Italy, R.D.M. Page, University of Glasgow, UK, J.R. Pannell, University of Oxford, UK, W. Powell, DuPont Agricultural Biotech, USA, J. Provan, Scottish Crop Research Institute, UK, F.J. Rumsey, The Natural History Museum, UK, W.T. Sincalir, The Scottish Agricultural College, UK, N. Soranzo, Scottish Crop Research Institute, UK, C.A. Stace, University of Leicester, UK, B. Stoebe, Heinrich-Heine-Universitat Dusseldorf, Germany, J.C. Vogel, The Natural History Museum, UK, N.J. Wilson, Scottish Crop Research Institute, UK, K. Wolff, The University of Newcastle upon Tyne, UK, E.A. Zimmer, Laboratory of Molecular Systematics, USA.

Pteridosperms are the backbone of seed-plant phylogeny

Abstract Hilton J. (School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK) and R. M. Bateman (Natural History Museum, Cromwell Road, London, SW7 5BD, UK). Pteridosperms are the backbone of seed-plant phylogeny. J. Torrey Bot. Soc. 133: 119–168. 2006.— Using Doyle (1996) as a starting point, we compiled a morphological cladistic matrix of 54 coded taxa (31 wholly extinct, and 23 at least partly extant) and 102 informative characters in order to explore relationships among gymnosperms in general and pteridosperms in particular. Our core analysis omitted six supplementary fossil taxa and yielded 21 most-parsimonious trees that generated two polytomies in the strict consensus tree, both among pteridosperms; the first affected several hydraspermans, and the second affected the three peltasperm/ corystosperm taxa analyzed. The resulting topology broadly resembled topologies generated during previous morphological cladistic analyses that combined substantial numbers of extant and extinct higher taxa. Each of the five groups that include extant taxa was relatively well resolved as monophyletic and yielded the familiar Anthophyte topology (cycads (Ginkgo (conifers (Gnetales, angiosperms)))), strongly contradicting most recent DNA-based studies that placed Gnetales as sister to, or within, conifers. These five extant groups were embedded in the derived half of a morphologically diverse spectrum of extinct taxa that strongly influenced tree topology and elucidated patterns of acquisition of morphological character-states, demonstrating that pteridosperms and other more derived “stem-group” gymnosperms are critical for understanding seed-plant relationships. Collapses in strict consensus trees usually reflected either combinations of data-poor taxa or “wildcard” taxa that combine character states indicating strongly contradictory placements within the broader topology. Including three progymnosperms in the analysis and identifying the aneurophyte progymnosperm as outgroup proved crucial to topological stability. An alternative progymnosperm rooting allowed angiosperms to diverge below cycads as the basalmost of the extant groups, a morphologically unintuitive position but one that angiosperms have occupied in several recent molecular studies. We therefore believe that such topologies reflect inadequate rooting, which is inevitable in analyses of seed plants that use only extant taxa where the outgroups can only be drawn from ferns and/or lycopsids, groups that are separated from extant seed-plants by a vast phylogenetic discontinuity that is bridged only by wholly fossil groups. Given the rooting problem, and the poverty of the hypotheses of relationship that can be addressed using only extant taxa, morphology-based trees should be treated as the initial phylogenetic framework, to subsequently be tested using molecular tools and employing not only molecular systematics but also evolutionary-developmental genetics to test ambiguous homologies. Among several possible circumscriptions of pteridosperms, we prefer those that imply paraphyly rather than polyphyly and exclude only one monophyletic group, providing one cogent argument for the inclusion of extant cycads in pteridosperms. Although pteridosperms cannot realistically be delimited as a monophyletic group, they remain a valuable informal category for the plexus of gymnosperms from which arose several more readily defined monophyletic groups of seed-plants. The ideal solution of recognizing several monophyletic groups, each of which combines a “crown-group” with one or more pteridosperms, is not yet feasible, due to uncertainties of relationship and difficulties to satisfactorily delimiting the resulting groups using reliable apomorphies. Exploration of the matrix demonstrated that coding all of the organs of a plant (extinct or extant) and dividing significantly polymorphic coded taxa are highly desirable, thereby justifying the substantial investment of time required to reconstruct individual conceptual whole plants from disarticulated fossil organs.

HETEROSPORY: THE MOST ITERATIVE KEY INNOVATION IN THE EVOLUTIONARY HISTORY OF THE PLANT KINGDOM

1 In aggregate, past discussions of heterospory and its role in the alternation of generations are riddled with ambiguities that reflect overlap of terms and concepts. Heterospory sensu lato can be analyzed more effectively if it is fragmented into a series of more readily defined evolutionary innovations: heterospory sensu stricto (bimodality of spore size), dioicy, heterosporangy, endospory, monomegaspory, endomegasporangy, integumentation, lagenostomy, in situ pollination, in situ fertilization, pollen tube formation, and siphonogamy (Tables 1, 2, Figs 1, 13). Current evidence suggests that the last five characters are confined to the seed‐plants. 2 The fossil record documents repeated evolution of heterosporous lineages from anisomorphic homosporous ancestors. However, interpretation is hindered by disarticulation of fossil sporophytes, the difficulty of relating conspecific but physically independent sporophyte and gametophyte generations in free‐sporing pteridophytes, the inability to directly observe ontogeny, and the rarity of preservation of transient and/or microscopic reproductive phenomena such as syngamy and siphonogamy. Unfortunately, the rarely preserved phenomena are often of far greater biological significance than corresponding readily preserved phenomena (e.g. heterospory versus dioicy, heterosporangy versus endospory). 3 In most fossils gametophyte gender can only be inferred by extrapolation from the morphology of the sporophyte and especially of the spores. This is readily achieved for species possessing high‐level heterospory, when the two spore genders have diverged greatly in size, morphology, ultrastructure and developmental behaviour. However, the earliest stages in the evolution of heterospory, which are most likely to be elucidated in the early fossil record of land‐plants, also show least sporogenetic divergence. It is particularly difficult to distinguish large microspores and small megaspores from the large isospores of some contemporaneous homosporous species (Figs 3–6 a, g). Heterospory is best identified in fossils by quantitative analysis of intrasporangial spore populations. 4 The spatial scale of the differential expression of megaspores and microspores varies from co‐occurrence in a single sporangium (anisospory) to different sporophytes (dioecy) (Figs 6–8). Studies of the relative positions of the two spore morphs on the sporophyte, and of developmentally anomalous terata (Fig. 9), demonstrate that gender is expressed epigenetically in both the sporophyte and gametophyte. Hormonal control operates via nutrient clines, with nutrient‐rich microenvironments favouring femaleness; megaspores and microspores compete for sporophytic resources. External environments can also influence gender, particularly in free‐living exosporic gametophytes. 5 The evolution of heterospory was highly iterative. The number of origins is best assessed via cladograms, but no current phylogeny includes sufficient relevant tracheophyte species. Also, several extant heterosporous species differ greatly from their closest relatives due to high degrees of ecological specialization and/or saltational evolution; extensive molecular data will be needed to ascertain their correct phylogenetic position. Current evidence suggests a minimum of 11 origins of heterospory, in the Zosterophyllopsida (1: Upper Devonian), Lycopsida (1: Upper Devonian), Sphenopsida (?2: Lower Carboniferous), Pteropsida (?4: Upper Cretaceous/Palaeogene) and Progymnospermopsida (?3: Upper Devonian/Carboniferous). The arguably monophyletic Gymnospermopsida probably inherited heterospory from their progymnospermopsid ancestor (Table 3, Figs 11–13). No origin of heterospory coincides with the origin of (and thus delimits) any taxonomic class of tracheophytes. The actual number of origins of heterospory is probably appreciably higher, exceeding that of any other key evolutionary innovation in land‐plants and offering an unusually good opportunity to infer evolutionary process from pattern. 6 Heterospory reflects the convergent attainment of similar modes of reproduction in phylogenetically disparate lineages. Nature repeated this experiment many times, whereas true phylogenetic synapomorphies evolve only once and require a unique causal explanation. Cladograms also offer the best means of determining the sequence of acquisition of heterosporic phenomena within lineages, here exemplified using the lycopsids (Fig. 10). Comparison of such sequences among lineages can potentially allow generalizations about underlying evolutionary mechanisms. Current evidence (albeit inadequate) indicates broadly similar sequences of character acquisitions in all lineages, though they differ in detail. Some logical evolutionarily stages were temporarily bypassed. Other lineages appear to have acquired two or more characters during a single saltational evolutionary event. Heterosporic phenomena can also be lost during evolution. Although no complete reversals to homospory have been documented, this could reflect unbreakable developmental canalization of heterospory rather than selective advantage relative to homospory. Several extant species refute widely held assumptions that certain phenomena, notably heterospory and dioicy, are reliably positively correlated. Moreover, some fossils are likely to possess combinations of heterosporic characters that are not found in their extant descendants. Fossil data have played a crucial role in understanding both the number of origins of heterospory and the ensuing patterns of character acquisition. 7 Although non‐adaptive evolutionary events are likely in at least some lineages, the highly iterative nature of heterospory and similar patterns of character acquisition in different lineages together suggest that its evolution was largely adaptively driven. However, many previous adaptive models of heterosporic evolution confused pattern and process, and paid insufficient attention to the role of the environment as a passive filter of novel morphotypes. Linear gradualistic models were imposed on the data, often intercalating hypothetical intermediates where desired. 8 The evolution of heterospory is best understood in terms of inherent antagonism between the sporophytic and gametophytic phases of the life history for control of sex ratio and reproductive timing. Control is achieved directly by the gametophyte, via gametogenesis, and indirectly by the sporophyte, via sporogenesis and the ability to determine to varying degrees the environment in which the gametophyte undergoes sexual reproduction. Increasing levels of heterospory (particularly the acquisition of endospory) compress the heteromorphic life history, as the increasingly dominant sporophyte progressively co‐opts the sex determination role of the gametophyte. The resulting life history is more holistic, effectively streamlining evolution by offering only a single target for selection. 9 However, by wresting control of sex ratios from the gametophyte, the ability of the sporophyte to respond rapidly to environmental changes decreases. This competitive weakness is greatest for heterosporous species possessing exosporic but obligately unisexual gametophytes (epitomized by the pteropsid Platyzoma*). It can be alleviated in endosporic species by occupying favourable environments (e.g. the aquatic Salviniales and Marsileales), switching to an apomictic mode of reproduction (thereby incurring inbreeding depression; e.g. many selaginellaleans), or acquiring more complex pollination biologies (thereby by‐passing the environment as a selective filter: the seed‐plants). 10 Lineages differ greatly in the maximum number of heterosporic characters that were acquired by their most derived constituent species. Several Devono‐Carboniferous lineages reached the level of reducing numbers of functional megaspores to one per sporangium (Figs 7 e, f, 8, 13), but only the putatively monophyletic gymnospermopsids broke through this apparent barrier to acquire the increasingly complex pollination biology that characterizes modern seed‐plants. 11 Many theories have been proposed to explain the remarkable success (both in terms of species diversity and ecological dominance) of seed‐plants. The majority focus on characters that are absent from the earliest seed‐plants (the Devono‐Carboniferous lyginopterid pteridospermaleans), which were no more reproductively sophisticated than other penecontemporaneous lineages possessing advanced heterospory (particularly the most derived lycopsids, equisetaleans and progymnospermopsids). Reliable pollination was a key reproductive breakthrough, though the sophisticated economic‐vegetative characters inherited by the earliest seed‐plants from their putative progymnospermopsid ancestors were probably equally important in ensuring their success in water‐limited habitats. 12 With the exception of some ecologically specialized pteropsids, known heterosporous lineages originated during a relatively short period in the Upper Devonian and Carboniferous (Fig. 11). They exploited a window of opportunity that existed before niches became too finely partitioned and saturated with seed‐plant species. This non‐uniformitarian ecology renders negligible the probability of new heterosporous lineages becoming established today, even though ‘hopeful monsters’ possessing ‘incipient heterospory’ are probably constantly being generated from homosporous parents.

Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots

A gynostemium, comprising stamen filaments adnate to a syncarpous style, occurs in only three groups of monocots: the large family Orchidaceae (Asparagales) and two small genera Pauridia (Hypoxidaceae: Asparagales) and Corsia (Corsiaceae, probably in Liliales), all epigynous taxa. Pauridia has actinomorphic (polysymmetric) flowers, whereas those of Corsia and most orchids are strongly zygomorphic (monosymmetric) with a well‐differentiated labellum. In Corsia the labellum is formed from the outer median tepal (sepal), whereas in orchids it is formed from the inner median tepal (petal) and is developmentally adaxial (but positionally abaxial in orchids with resupinate flowers). Furthermore, in orchids zygomorphy is also expressed in the stamen whorls, in contrast to Corsia. In Pauridia a complete stamen whorl is suppressed, but the ‘lost’ outer whorl is fused to the style. The evolution of adnation and zygomorphy are discussed in the context of the existing phylogenetic framework in monocotyledons. An arguably typological classification of floral terata is presented, focusing on three contrasting modes each of peloria and pseudopeloria. Dynamic evolutionary transitions in floral morphology are assigned to recently revised concepts of heterotopy (including homeosis) and heterochrony, seeking patterns that delimit developmental constraints and allow inferences regarding underlying genetic controls. Current evidence suggests that lateral heterotopy is more frequent than acropetal heterotopy, and that full basipetal heterotopy does not occur. Pseudopeloria is more likely to generate a radically altered yet functional perianth, but is also more likely to cause acropetal modification of the gynostemium. These comparisons indicate that there are at least two key genes or sets of genes controlling adnation, adaxial stamen suppression and labellum development in lilioid monocots; at least one is responsible for stamen adnation to the style (i.e. gynostemium formation), and another controls adaxial stamen suppression and adaxial labellum formation in orchids. Stamen adnation to the style may be a product of over‐expression of the genes related to epigyny (i.e. a form of hyper‐epigyny). If, as seems likely, stamen‐style adnation preceded zygomorphy in orchid evolution, then the flowers of Pauridia may closely resemble those of the immediate ancestors of Orchidaceae, although existing molecular phylogenetic data indicate that a sister‐group relationship is unlikely. The initial radiation in Orchidaceae can be attributed to the combination of hyper‐epigyny, zygomorphy and resupination, but later radiations at lower taxonomic levels that generated the remarkable species richness of subfamilies Orchidoideae and Epidendroideae are more likely to reflect more subtle innovations that directly influence pollinator specificity, such as the development of stalked pollinaria and heavily marked and or spur‐bearing labella.

Stable Epigenetic Effects Impact Adaptation in Allopolyploid Orchids (Dactylorhiza: Orchidaceae)

Epigenetic information includes heritable signals that modulate gene expression but are not encoded in the primary nucleotide sequence. We have studied natural epigenetic variation in three allotetraploid sibling orchid species (Dactylorhiza majalis s.str, D. traunsteineri s.l., and D. ebudensis) that differ radically in geography/ecology. The epigenetic variation released by genome doubling has been restructured in species-specific patterns that reflect their recent evolutionary history and have an impact on their ecology and evolution, hundreds of generations after their formation. Using two contrasting approaches that yielded largely congruent results, epigenome scans pinpointed epiloci under divergent selection that correlate with eco-environmental variables, mainly related to water availability and temperature. The stable epigenetic divergence in this group is largely responsible for persistent ecological differences, which then set the stage for species-specific genetic patterns to accumulate in response to further selection and/or drift. Our results strongly suggest a need to expand our current evolutionary framework to encompass a complementary epigenetic dimension when seeking to understand population processes that drive phenotypic evolution and adaptation.

Experimental cladistic analysis of anatomically preserved arborescent lycopsids from the carboniferous of Euramerica : an essay on paleobotanical phylogenetics

This evolutionary cladistic analysis of the arborescent (wood-producing) lycopsids, an exclusively fossil group of vascular plants, is confined to the strongest available data: anatomically preserved fossils that have been painstakingly reconstructed into conceptual whole plants. Ten Carboniferous genera are represented by 16 species: four pseudoherbs/«shrubs» and 12 of the arboreous (tree-sized) species that epitomize the Pennsylvanian coal swamps of Euramerica. The 69 vegetative and 46 reproductive characters are described in detail; several key terms are redefined and homologies reassessed (...)

Population genetic structure in European populations of Spiranthes romanzoffiana set in the context of other genetic studies on orchids

Spiranthes romanzoffiana Cham. is restricted in Europe to the British Isles, where it is recognised as a conservation priority species due to frequent extirpation of populations along with no evidence of seed set; vegetative reproduction has been invoked as the sole means of perpetuation and dispersal. To investigate the reproductive ecology of this species, 17 populations have been sampled for chloroplast microsatellites and amplified fragment length polymorphisms (AFLPs). These markers revealed a previously unsuspected genetic–geographic split in the species, which correlates with differences in patterns of within-population variation. Northern populations were fixed for one chloroplast haplotype but showed high levels of AFLP genotypic diversity consistent with sexual reproduction (proportion of genotypes distinguishable, PD=0.98). More southerly populations showed fixed differences from the northern populations in their chloroplast haplotype and for 10 AFLP markers. They harboured only 12 unique multilocus genotypes among 113 individuals from six populations (PD=0.11). These genotypes differed mostly by single bands, and none by more than 4/138 loci, with identical multilocus genotypes occurring in widely separated populations. This uniformity in southern populations is consistent with agamospermous or autogamous reproduction, and/or an extreme population bottleneck. Finally, the observed patterns of population differentiation in S. romanzoffiana are compared with other studies of orchids, revealing a wide range of values that belie recent contrasting published generalisations that claim that orchids show either higher, or lower, levels of population differentiation than other plant families.

Partitioning and diversity of nuclear and organelle markers in native and introduced populations of Epipactis helleborine (Orchidaceae)

Variability of allozymes (1170 individuals, 47 populations) and chloroplast DNA (692 individuals, 29 populations) was examined in native European and introduced North American populations of Epipactis helleborine (Orchidaceae). At the species level, the percentage of allozyme loci that were polymorphic (P(99)) was 67%, with a mean of 2.11 alleles (A) per locus, and an expected heterozygosity (H(exp)) of 0.294. At the population level, mean P(99) = 56%, mean A = 1.81, and mean H(exp) = 0.231. Although field observations suggest that self-pollination occurs frequently, populations had a genetic structure consistent with Hardy-Weinberg expectations and random mating (mean F(IS) = 0.002). There was significant deviation from panmixia associated with population differentiation (mean F(ST) = 0.206). The distribution of two chloroplast haplotypes showed that 15 of the 29 populations were polymorphic. Using both nuclear and organelle F(ST) estimates, a pollen to seed flow ratio of 1.43 : 1 was calculated. This is very low compared with published estimates for other plant groups, consistent with the high dispersability of orchid seeds. Finally, there was no evidence for a genetic bottleneck associated with the introduction of E. helleborine to North America.

Evolution and temporal diversification of western European polyploid species complexes in Dactylorhiza (Orchidaceae)

Patterns of polyploid evolution in the taxonomically controversial Dactylorhiza incarnata/maculata groups were inferred genetically by analyzing 399 individuals from 177 localities for (1) four polymorphic plastid regions yielding aggregate haplotypes and (2) nuclear ribosomal ITS allele frequencies. Concordance between patterns observed in distributions of plastid haplotypes and ITS alleles renders ancestral polymorphism an unlikely cause of genetic variation in diploids and allopolyploids. Combining the degree of concerted evolution in ITS alleles (thought to reflect gene conversion) with inferred parentage provides support for a quadripartite classification of western European allopolyploid dactylorchids according to their respective parentage and relative dates of origin. The older allotetraploids that generally exhibit only one parental ITS allele can be divided into those derived via hybridization between the divergent complexes we now call D. incarnata s.l. and D. fuchsii (e.g., D. majalis) and those derived via hybridization between D. incarnata s.l. and D. maculata (e.g., D. elata). Similarly, the younger allotetraploids that maintain evidence of both parental ITS alleles can be divided into those derived from hybridization between D. incarnata s.l. and D. fuchsii, or perhaps in some cases a diploid species resembling D. saccifera (e.g., D. praetermissa, D. purpurella, D. traunsteineri s.l., D. baltica), and those derived from hybridization between the D. incarnata s.l. and D. maculata groups (e.g., D. occidentalis, D. sphagnicola). Older allotetraploids are inferred to have passed through glacially induced migration bottlenecks in southern Eurasia, whereas at least some younger allotetraploids now occupying northern Europe are inferred to have originated post-glacially and remain sympatric with their parents, a scenario that is largely in agreement with the morphology and ecology of these allotetraploids. ITS conversion is in most cases biased toward the maternal parent, eventually obscuring evidence of the original allopolyploidization event because plastid haplotypes also reflect the maternal contribution. Gene flow appears unexpectedly low among allotetraploids relative to diploids, whereas several mechanisms may assist the gene flow observed across ploidy levels. There is good concordance between (1) the genetically delimited species that are required to accurately represent the inferred evolutionary events and processes and (2) morphologically based species recognized in certain moderately conservative morphological classifications previously proposed for the genus. Further research will seek to improve sampling, especially in eastern Eurasia, and to develop more sensitive markers for distinguishing different lineages within (1) the remarkably genetically uniform D. incarnata group (diploids) and (2) locally differentiated populations of (in some cases unnamed) allotetraploids. (Less)

EVOLUTIONARY-DEVELOPMENTAL CHANGE IN THE GROWTH ARCHITECTURE OF FOSSIL RHIZOMORPHIC LYCOPSIDS: SCENARIOS CONSTRUCTED ON CLADISTIC FOUNDATIONS

The Rhizomorphales, the most derived portion of the lycopsid (clubmoss) Glade, is now represented only by the diminutive genus Isoetes. However, during their Late Palaeozoic acme the rhizomorphic lycopsids exhibited a wide range of architectures and body sizes, from recumbent pseudoherbs to trees 40 m high. All possessed the rhizomorphic syndrome: a centralized rootstock and secondary thickening, reflecting an inescapable developmental constraint of bipolar determinate growth. These features in turn allowed acquisition of the tree habit by the lycopsids, independently of the physiologically and ontogenetically distinct lignophyte Glade that includes the seed‐plants. Differences among lycopsid genera in the number and size of four major growth modules – rhizomorph, stem, lateral branches (two positionally distinct submodules), and isotomous crown branches – resulted from differences in the relative size, number and equality of dichotomies of the apical meristems.