Thomas Denk

Episodic migration of oaks to Iceland: Evidence for a North Atlantic “land bridge” in the latest Miocene

Dating the subsidence history of the North Atlantic Land Bridge (NALB) is crucial for understanding intercontinental disjunctions of northern temperate trees. Traditionally, the NALB has been assumed to have functioned as a corridor for plant migration only during the early Cenozoic, but recent findings of plant fossils and inferences from molecular studies are challenging this view. Here, we report dispersed pollen of Quercus from Late Miocene sediments in Iceland that shows affinities with extant northern hemispheric white oaks and North American red oaks. Older (15 to 10 Ma) sediments do not contain pollen of Quercus suggesting it arrived after that time. Pollen from the 9-8 Ma Hrútagil locality is indistinguishable from morphotypes common among white and red oaks. In contrast, pollen from the 5.5 Ma Selárgil locality has a tectum that is at present confined to North American white and red oaks, indicating a second episode of migration to Iceland. These findings suggest that transatlantic migration of temperate plant taxa may not have been limited by vast areas of sea or by cold climates during the Miocene. Furthermore, our results offer a plausible explanation for the remarkably low degree of genetic differentiation between modern disjunct European and North American oaks.

The evolutionary history of Fagus in western Eurasia: Evidence from genes, morphology and the fossil record

Abstract. Fagus (beech) is among the most abundant and economically important genera of broad-leaved trees in northern hemisphere temperate forests. The number of modern taxa present in Europe and Asia Minor has long been a matter of debate and up to five species have been recognised. To resolve taxonomic and phylogenetic relationships we conducted morphological and molecular genetic analyses in western Eurasiatic taxa and evaluated palaeontological evidence. To place our findings from western Eurasiatic populations in a broader context additional East Asiatic and North American species of the same subgenus Fagus as well as two species of the subgenus Engleriana were included in our study.The morphological features exhibited in western Eurasiatic populations of Fagus show a west-east gradient that is characterised by strongly overlapping variability between geographical races. Fagus populations from Asia Minor exhibit an even higher variability that is also reflected in their genetic variability of nuclear rDNA internal transcribed spacer (ITS) sequences. The intraspecific genetic variability recorded here is in conflict with previous ITS studies in Fagus. The high amount of ITS polymorphism within Fagus from western Eurasia along with the clinal variation observed for morphological characters suggest the presence of only a single species, Fagus sylvatica L., in Europe and Asia Minor. Previously recognised taxa such as F. orientalis Lipsky and Fagus moesiaca (Malý) Czeczott should therefore be treated as synonyms of Fagus sylvatica. Although species belonging to the subgenus Engleriana were genetically distinct from species of the subgenus Fagus, relationships within the subgenus Fagus could not be clearly resolved. A reason for this could be the low rate of diversification in Fagus during the early phase of range expansion of the genus in the Oligocene period as indicated by the uniformity of leaf and cupule/nut fossils. This may account for the low overall ITS divergence and the high degree of polymorphism encountered in the subgenus Fagus and points to a late differentiation of western Eurasiatic and eastern Asiatic species. Area disruptions during the Pleistocene and the post-glacial recolonisation of western Europe appear to have caused the west-east gradient that is apparent in modern Fagus of western Eurasia but absent in Late Tertiary ancestors of Fagus sylvatica.

Significance of Pollen Characteristics for Infrageneric Classification and Phylogeny in Quercus (Fagaceae)

Patterns of tectum ornamentation in pollen of Quercus (oak trees, Fagaceae) are investigated using high‐resolution scanning electron microscopy. Tectum ornamentation is highly consistent at the infrageneric level and can be used to polarize character states within Quercus by comparison with other genera in Fagaceae. In particular, pollen data strongly suggest the recognition of an infrageneric Ilex group and, for the first time, allow definition of the set of taxa that comprise this group. The infrageneric Ilex group displays a relatively simple tectum ornamentation exclusively found in this group of oaks, in Fagus, and in extinct lineages related to Trigonobalanus, Colombobalanus, and Formanodendron. Such a simple type of tectum ornamentation is also known to represent an early developmental stage in infrageneric groups of Quercus that have otherwise complex ornamentation (Quercus and Lobatae). Ornamentation of the tectum in the infrageneric Cyclobalanopsis group can be derived from the plesiomorphic Ilex type showing little accumulation of secondary sporopollenin. In the infrageneric Cerris, Protobalanus, Quercus, and Lobatae groups, accumulation of secondary sporopollenin masks the basic Ilex pattern. The five distinct types of tectum ornamentation are in perfect agreement with published molecular phylogenies of Quercus. Thus, pollen ornamentation is a most valuable tool to identify members of the major infrageneric groups in Quercus and provides the basis for a reevaluation of the fossil record of Quercus.

Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications

To study phylogenetic relationships among species of Fagus, the internal transcribed spacer regions ITS1 and ITS2 of the nuclear ribosomal DNA and morphological data were analyzed. Both molecular and morphologically based phylogenies suggest that Eurasian species of Fagus subgenus Fagus are basal to the North American Fagus grandifolia. The subgenus Fagus is a paraphyletic group basal to three East Asian species forming the subgenus Engleriana. Due to a considerably large amount of DNA polymorphism, relationships among basal species of Fagus could not be entirely resolved when analyzing ITS sequences with standard methods. Morphological trees helped to resolve more clearly relationships within the subgenus Fagus. The East Asian F. hayatae is suggested to be basal to the rest of the genus. This hypothesis is further supported by distinctive patterns of nucleotide variability found for ITS regions, allowing for basic and derived types to be distinguished. The high degree of ITS polymorphism within Fagus can be explained by (1) the complex evolutionary behavior of this marker, (2) the stenoecious ecological characteristic of Fagus with respect to its continuous geographic range throughout much of the Cenozoic, and (3) the absence of major radiations into further habitats as occurred in other Fagaceae.

A Late Devonian arborescent lycopsid Sublepidodendron songziense Chen emend. (Sublepidodendraceae Krausel et Weyland 1949) from China, with a revision of the genus Sublepidodendron (Nathorst) Hirmer 1927

Abstract The study of a Late Devonian arborescent lycopsid, Sublepidodendron songziense Chen 1977, from the Hsiehchingssu (Xiejingsi) Formation of Hubei Province and the Wutung (Wutong) Formation of Anhui Province, PR China, provides new insight into its holistic architecture and taxonomic affinity. The study allows several interrelated organ species to be integrated into a conceptual whole-plant species, Sublepidodendron songziense Chen emend. Wang Q., Hao, Wang D.-M., Wang Y. et Thomas Denk. The plant consists of a monocaulous trunk growing from a stigmarian rhizomorph, the trunk bearing biseriate, sub-opposite to possibly alternate lateral branches that expand by means of isotomous to slightly anisotomous dichotomies, forming an excurrent canopy. Lateral branches bear terminal Lepidostrobus -like strobili. These strobili are dimorphic, implying separate mega- and microsporangiate strobili considered with the associated organ assemblage, including Triletes -type megaspores, Lepidocarpopsis -like sporophylls, and Lepidophloios -like cauline anatomy. Moreover, lateral branches are caducous, and ulodendroid scars mark the attachment sites of former branches onto the trunk. The plant diagnostically possesses spirally arranged, small, vertically elongated leaf cushions, which have false leaf scars. The presence of ligule cannot be excluded definitely. The characteristics of leaf cushions show considerable variation corresponding to different taphonomic processes, preservational modes and ontogenetic stages so that this plant megafossil has been classified in various ways previously. Based on organic connection and cauline anatomy, a reconstruction of the whole-plant species is tentatively given. We compare this whole-plant species to the type species S. mirabile (Nathorst) Hirmer, and revise Sublepidodendron (Nathorst) Hirmer 1927, suggesting that the genus and its own family Sublepidodendraceae sensu Krausel et Weyland 1949 should be separated from the order Protolepidodendrales sensu Pichi-Sermolli 1958 and referred to the order Isoetales sensu lato and the suborder Dichostrobiles sensu DiMichele et Bateman 1996. Present Ulodendron specimens are the earliest record in the Late Palaeozoic strata, demonstrating that the pseudomonopodial branching architectural form in the arboresent lycopsids had evolved by the Late Devonian (Famennian). Such a woody trunk together with lateral branches (or cauline peduncles), separate mega- and microsporangiate strobili, and rootlet-bearing rhizomorph epitomize the major structural units (or architectural modules) of a true arborescent lycopsid, and S. songziense appears to be the oldest arborescent lycopsid showing an apparently centralized rhizomorph. We suggest that phylogenetically more advanced arborescent lycopsids did not precipitately occur in the Carboniferous, rather they had already evolved by the Late Devonian (Famennian). The widespread genus Sublepidodendron (Nathorst) Hirmer 1927 emend., especially abundant in China, among the Late Devonian–Early Carboniferous floras may represent one of the progenitors of the phylogenetically advanced arborescent lycopsids.

Pollen, fruits, and leaves of Tetracentron (Trochodendraceae) from the Cainozoic of Iceland and western North America and their palaeobiogeographic implications

Dispersed pollen, fruits, and leaves of Tetracentron (Trochodendraceae) are described from the Miocene of Iceland and assigned to a new species, Tetracentron atlanticum. The Icelandic fossils represent the first unambiguous record of Tetracentron for the Cainozoic of Europe. Well‐preserved dispersed grains of Tetracentron are also identified from the Eocene and Miocene of western North America and compared to the Icelandic fossils. In general, Tetracentron pollen is rather uniform through the Eocene to Recent, only displaying minor variation in ornamentation. Leaves are diagnostic at the species level. The findings add substantial new information to the generally poor fossil record of Tetracentron and indicate a more circumpolar distribution of the genus than previously assumed. The north‐eastern Asian – western North American Cainozoic distribution for plant taxa presently confined to East Asia is relatively common. In contrast, the extension to Iceland is remarkable, particularly in view of the absence of the genus in the fossil record from eastern North America, Greenland, and Central Asia and mainland Europe.

First evidence of epidermal structures of Ginkgo from the Mediterranean Tertiary

Abstract Tertiary leaf compressions of a Ginkgo plant with cuticle displaying all taxonomically important epidermal features are reported for the first time from Greece, and for the Mediterranean area as a whole. The fossils are from Upper Miocene sediments of Vegora, north-western Greece, and assigned to Ginkgo adiantoides (Unger) Heer. The most conspicuous cuticle characteristics are prominent papillae on the subsidiary cells that sometimes completely cover the stomatal apertures. Such papillae also occur in leaves of G. adiantoides from the Pliocene of eastern Central Europe, but are absent in leaves from the Pliocene of Germany also assigned to this species. We observed a high variability in the degree of papillosity of subsidiary cells of stomata in leaves of living Ginkgo biloba that exhibited prominent papillae in mature sun leaves and a total lack of papillae in shade leaves of a potted plant. This may suggest that differences in epidermal characters between the fossil leaves from Greece and Germany are due to ecotypical/intraspecific variability and not to genetically fixed specific differences. It also suggests that a number of Tertiary Ginkgo species from Eurasia that were distinguished from G. adiantoides by having papillate epidermis cells and subsidiary cells of the abaxial cuticle should be included within G. adiantoides . Two lineages of Ginkgo can be distinguished for the Tertiary of the Northern Hemisphere. From the Palaeogene high latitudes leaves were reported that exhibit upper epidermis cells with prominent papillae similar to those of older Mesozoic Ginkgo , whereas G. adiantoides lacks the papillae of the upper epidermis, a feature which is shared with the living G. biloba . In general, the size of stomata is larger in extant Ginkgo leaves than in those of the fossils.

Fagaceae pollen from the early Cenozoic of West Greenland: revisiting Engler’s and Chaney’s Arcto-Tertiary hypotheses

In this paper we document Fagaceae pollen from the Eocene of western Greenland. The pollen record suggests a remarkable diversity of the family in the early Cenozoic of Greenland. Extinct Fagaceae pollen types include Eotrigonobalanus, which extends at least back to the Paleocene, and two ancestral pollen types with affinities to the Eurasian Quercus Group Ilex and the western North American Quercus Group Protobalanus. In addition, modern lineages of Fagaceae are unambiguously represented by pollen of Fagus, Quercus Group Lobatae/Quercus, and three Castaneoideae pollen types. These findings corroborate earlier findings from Axel Heiberg Island that Fagaceae were a dominant element at high latitudes during the early Cenozoic. Comparison with coeval or older mid-latitude records of modern lineages of Fagaceae shows that modern lineages found in western Greenland and Axel Heiberg likely originated at lower latitudes. Further examples comprise (possibly) Acer, Aesculus, Alnus, Ulmus, and others. Thus, before fossils belonging to modern northern temperate lineages will have been recovered from older (early Eocene, Paleocene) strata from high latitudes, Engler’s hypothesis of an Arctic origin of the modern temperate woody flora of Eurasia, termed ‘Arcto-Tertiary Element’, and later modification by R. W. Chaney and H. D. Mai (‘Arcto-Tertiary Geoflora’) needs to be modified.

Plastome data reveal multiple geographic origins of Quercus Group Ilex

Nucleotide sequences from the plastome are currently the main source for assessing taxonomic and phylogenetic relationships in flowering plants and their historical biogeography at all hierarchical levels. One major exception is the large and economically important genus Quercus (oaks). Whereas differentiation patterns of the nuclear genome are in agreement with morphology and the fossil record, diversity patterns in the plastome are at odds with established taxonomic and phylogenetic relationships. However, the extent and evolutionary implications of this incongruence has yet to be fully uncovered. The DNA sequence divergence of four Euro-Mediterranean Group Ilex oak species (Quercus ilex L., Q. coccifera L., Q. aucheri Jaub. & Spach., Q. alnifolia Poech.) was explored at three chloroplast markers (rbcL, trnK/matK, trnH-psbA). Phylogenetic relationships were reconstructed including worldwide members of additional 55 species representing all Quercus subgeneric groups. Family and order sequence data were harvested from gene banks to better frame the observed divergence in larger taxonomic contexts. We found a strong geographic sorting in the focal group and the genus in general that is entirely decoupled from species boundaries. High plastid divergence in members of Quercus Group Ilex, including haplotypes shared with related, but long isolated oak lineages, point towards multiple geographic origins of this group of oaks. The results suggest that incomplete lineage sorting and repeated phases of asymmetrical introgression among ancestral lineages of Group Ilex and two other main Groups of Eurasian oaks (Cyclobalanopsis and Cerris) caused this complex pattern. Comparison with the current phylogenetic synthesis also suggests an initial high- versus mid-latitude biogeographic split within Quercus. High plastome plasticity of Group Ilex reflects geographic area disruptions, possibly linked with high tectonic activity of past and modern distribution ranges, that did not leave imprints in the nuclear genome of modern species and infrageneric lineages.

Comparative pollen morphology and ultrastructure of Platanus: Implications for phylogeny and evaluation of the fossil record

Pollen of Platanus was studied using light (LM) and electron microscopy (SEM and TEM). Overall, pollen is uniform in modern Platanus (small, tricolpate, prolate to spheroidal, reticulate, semitectate). A number of characters, however, display remarkable variability within a taxon and even a single anther (size; foveo‐reticulate, fine to coarse reticulate ornamentation). Platanus kerrii (subgenus Castaneophyllum) differs from the remaining species by its high and “folded” reticulum and possibly the smooth colpus membrane. Moreover, to our knowledge, pollen of the P. kerrii – type is not known from the fossil record. The exine in modern and fossil Platanaceae shows great structural similarity, but the thickness of the foot layer within the ectexine is less variable and normally smaller in modern taxa. Furthermore, in Early Cretaceous to Early Cainozoic Platanaceae a number of distinct pollen types occurred that are not known within the modern Platanus. Considering pollen of Platanaceae from the Early Cretaceous to today, a dynamic picture of the evolution of the family emerges. In the first phase (Early Cretaceous) pollen of extinct genera such as Aquia differed considerably from modern Platanus and shows strong similarity to basal eudicot taxa such as Ranunculales (e.g. Lardizabalaceae). The Late Cretaceous Platananthus hueberi displays a distinct coarse reticulum that is unknown from modern Platanus but similar to some taxa of Hamamelidaceae (e.g. Exbucklandia). After the first phase of eudicot radiation that appears to have been characterized by strongly reticulate evolution, platanaceous diversity decreased in the course of the Cainozoic. Despite this, the pollen type of the modern subgenus Castaneophyllum (P. kerrii type) seems to be an innovation that originated after the initial radiation of the family.