Mongolitria: A new Early Cretaceous three-valved seed from Northeast Asia.

PREMISE: Fossil seeds recovered from the Early Cretaceous of Mongolia and Inner Mongolia, China, are described and assigned to Mongolitria gen. nov., a new genus of gymnosperm seed. METHODS: Abundant lignitized seeds along with compression specimens isolated from the matrix were studied using a combination of scanning electron microscopy, anatomical sectioning, light microscopy, synchrotron radiation X-ray microtomography, and cuticle preparations. A single permineralized seed was examined by light microscopy of cellulose acetate peels and X-ray microtomography. RESULTS: Two species are recognized, Mongolitria friisae sp. nov. and Mongolitria exesum sp. nov. Both seeds are orthotropous with a short apical micropyle and a small, basal, circular attachment scar. The thick sclerenchymatous integument has a consistently three-parted organization and about 20 conspicuous longitudinal ribs on the surface. Mongolitria exesum differs from M. friisae primarily in its much larger size and thicker seed coat, which also preserves clear evidence of insect damage. CONCLUSIONS: Mongolitria is similar to other fossil seeds that have been assigned to Cycadales, but displays a unique combination of characters not found in any living or extinct cycadaceous plant, leaving its higher-level systematic affinities uncertain. Germination apparently involved splitting of the integument into three valves. Mongolitria was prominent among the plant parts accumulating in peat swamps in eastern Asia during the Early Cretaceous.

First evidence of a monodominant (Englerodendron, Amherstieae, Detarioideae, Leguminosae) tropical moist forest from the early Miocene (21.73 Ma) of Ethiopia.

Many tropical wet forests are species-rich and have relatively even species frequency distributions. But, dominance by a single canopy species can also occur in tropical wet climates and can remain stable for centuries. These are uncommon globally, with the African wet tropics supporting more such communities than the Neotropics or Southeast Asia. Differences in regional evolutionary histories are implied by biogeography: most of Africa's monodominance-forming species are Amherstieae-tribe legumes; monodominance in Neotropical forests occur among diverse taxonomic groups, often legumes, but rarely Amherstieae, and monodominance in Southeast Asian forests occurs mostly among Dipterocarpaceae species. African monodominant forests have been characterized ecologically and taxonomically, but their deep-time history is unknown despite their significant presence and bottom-up ecological influence on diversity. Herein we describe fossil leaflets of Englerodendron mulugetanum sp. nov., an extinct species of the extant genus Englerodendron (Berlinia Clade, Amherstieae, Detarioideae) from the 21.73 Ma Mush Valley site in Ethiopia. We also document a detailed study of associated legume pollen, which originate from a single taxon sharing characters with more than one extant descendant. Taxonomically, the pollen is most comparable to that from some extant Englerodendron species and supports a likely affiliation with the Englerodendron macrofossils. The Mush Valley site provides the first fossil evidence of a monodominant tropical forest in Africa as represented by leaflets and pollen. Previous studies documented >2400 leaves and leaflets from localities at six stratigraphic levels spanning 50,000-60,000 years of nearly continuous deposition within seven meters of section; all but the basal level contain ≥ 50% E. mulugetanum leaflets. Modern leaf litter studies in African mixed vs. monodominant forests indicates the likelihood of monodominance in the forests that surrounded the Mush paleolake, particularly after the basal level. Thus, we provide an early case for monodominance within the Amherstieae legumes in Africa.

A permineralized Early Cretaceous lycopsid from China and the evolution of crown clubmosses.

Lycopodiaceae are one of three surviving families of lycopsids, a lineage of vascular plants with a fossil history dating to at least the Early Devonian or perhaps the Late Silurian (c. 415 Ma). Many fossils have been linked to crown Lycopodiaceae, but the lack of well-preserved material has hindered definitive recognition of this group in the paleobotanical record. New, exceptionally well-preserved permineralized lycopsid fossils from the Early Cretaceous (125.6 ± 1.0 Ma) of Inner Mongolia, China, were examined in detail using acetate peel and micro-computed tomography techniques. The anatomy of extant Lycopodiaceae was analyzed for comparison using fluorescence microscopy. Phylogenetic relationships of the new fossil to extant Lycopodiaceae were evaluated using parsimony and maximum likelihood analyses. Lycopodicaulis oellgaardii gen. et sp. nov. provides the earliest unequivocal and best-documented evidence of crown Lycopodiaceae and Lycopodioideae, based on anatomically-preserved fossil material. Recognition of Lycopodicaulis in Asia during the Early Cretaceous indicates the presence of crown Lycopodiaceae at this time, and striking similarities of stem anatomy with extant species provide a framework for the understanding of the interaction of branching and vascular anatomy in crown-group lycopsids.

Fossil papilionoids of the Bowdichia clade (Leguminosae) from the Paleogene of North America.

PREMISE: Understanding the evolutionary history of flowering plants has been enriched by the integration of molecular phylogenies and evidence from the fossil record. Fossil fruits and leaves from the late Paleocene and Eocene of Wyoming and Eocene of Kentucky and Tennessee are described as extinct genera in the tropical American Bowdichia clade of the legume subfamily Papilionoideae. Recent phylogenetic study and taxonomic revision of the Bowdichia clade have facilitated understanding of relationships of the fossil taxa and their evolutionary implications and paleoenvironmental significance. METHODS: The fossils were studied using standard methods of specimen preparation and light microscopy and compared to fruits and leaves from extant legume taxa using herbarium collections. Phylogenetic relationships of the fossil taxa were assessed using morphology and DNA sequence data. RESULTS: Two new fossil genera are described and their phylogenetic relationships are established. Paleobowdichia lamarensis is placed as sister to the extant genus Bowdichia and Tobya claibornensis is placed with the extant genera Guianodendron and Staminodianthus. CONCLUSIONS: These fossils demonstrate that the tropical American Bowdichia clade was present in North America during a period when tropical or subtropical conditions prevailed in the northern Rocky Mountains during the late Paleocene and the Mississippi Embayment during the middle Eocene. These fossils also document that the Bowdichia clade had diversified by the late Paleocene when the fossil record of the family is relatively sparse. This result suggests that future work on early fossil legumes should focus on tropical and subtropical climatic zones, wherever they may occur latitudinally.

Early Cretaceous abietoid Pinaceae from Mongolia and the history of seed scale shedding.

PREMISE: Seed cones of extant Pinaceae exhibit two mechanisms of seed release. In "flexers" the cone scales remain attached to the central axis, while flexing and separating from each other to release the seeds. In "shedders" scales are shed from the axis, with the seeds either remaining attached to the scale or becoming detached. The early fossil history of Pinaceae from the Jurassic to Early Cretaceous is dominated by flexing seed cones, while the systematic information provided by shedding fossil cones has been overlooked and rarely integrated with data based on compression and permineralized specimens. We describe the earliest and best-documented evidence of a "shedder" seed cone from the Aptian-Albian of Mongolia. METHODS: Lignite samples from Tevshiin Govi locality were disaggregated in water, washed, and dried in air. Fossils were compared to material of extant Pinaceae using LM and CT scans. RESULTS: Lepidocasus mellonae gen. et sp. nov. is characterized by a seed cone that disarticulated at maturity and shed obovate bract-scale complexes that have a distinctive ribbed surface and an abaxial surface covered with abundant trichomes. The ovuliferous scale has ca. 30-40 resin canals, but only scarce xylem near the attachment to the cone axis. Resin vesicles are present in the seed integument. Phylogenetic analysis places Lepidocasus as sister to extant Cedrus within the abietoid grade. CONCLUSIONS: The exquisite preservation of the trichomes in L. mellonae raises questions about their potential ecological function in the cones of fossil and living Pinaceae. Lepidocasus mellonae also shows that a shedding dispersal syndrome, a feature that has often been overlooked, evolved early in the history of Pinaceae during the Early Cretaceous.

Mesozoic cupules and the origin of the angiosperm second integument.

The second integument of the angiosperm ovule is unique among seed plants, with developmental genetics that are distinct from those of the inner integument1. Understanding how the second integument should be compared to structures in other seed plants is therefore crucial to resolving the long-standing question of the origin of angiosperms2-6. Attention has focused on several extinct plants with recurved cupules that are reminiscent of the anatropous organization of the basic bitegmic ovules of angiosperms1-6, but interpretations have been hampered by inadequate information on the relevant fossils. Here we describe abundant exceptionally well-preserved recurved cupules from a newly discovered silicified peat dating to the Early Cretaceous epoch (around 125.6 million years ago) in Inner Mongolia, China. The new material, combined with re-examination of potentially related fossils, indicates that the recurved cupules of several groups of Mesozoic plants are all fundamentally comparable, and that their structure is consistent with the recurved form and development of the second integument in the bitegmic anatropous ovules of angiosperms. Recognition of these angiosperm relatives (angiophytes) provides a partial answer to the question of angiosperm origins, will help to focus future work on seed plant phylogenetics and has important implications for ideas on the origin of the angiosperm carpel.

The Origin of the Legumes is a Complex Paleopolyploid Phylogenomic Tangle Closely Associated with the Cretaceous-Paleogene (K-Pg) Mass Extinction Event.

The consequences of the Cretaceous-Paleogene (K-Pg) boundary (KPB) mass extinction for the evolution of plant diversity remain poorly understood, even though evolutionary turnover of plant lineages at the KPB is central to understanding assembly of the Cenozoic biota. The apparent concentration of whole genome duplication (WGD) events around the KPB may have played a role in survival and subsequent diversification of plant lineages. To gain new insights into the origins of Cenozoic biodiversity, we examine the origin and early evolution of the globally diverse legume family (Leguminosae or Fabaceae). Legumes are ecologically (co-)dominant across many vegetation types, and the fossil record suggests that they rose to such prominence after the KPB in parallel with several well-studied animal clades including Placentalia and Neoaves. Furthermore, multiple WGD events are hypothesized to have occurred early in legume evolution. Using a recently inferred phylogenomic framework, we investigate the placement of WGDs during early legume evolution using gene tree reconciliation methods, gene count data and phylogenetic supernetwork reconstruction. Using 20 fossil calibrations we estimate a revised timeline of legume evolution based on 36 nuclear genes selected as informative and evolving in an approximately clock-like fashion. To establish the timing of WGDs we also date duplication nodes in gene trees. Results suggest either a pan-legume WGD event on the stem lineage of the family, or an allopolyploid event involving (some of) the earliest lineages within the crown group, with additional nested WGDs subtending subfamilies Papilionoideae and Detarioideae. Gene tree reconciliation methods that do not account for allopolyploidy may be misleading in inferring an earlier WGD event at the time of divergence of the two parental lineages of the polyploid, suggesting that the allopolyploid scenario is more likely. We show that the crown age of the legumes dates to the Maastrichtian or early Paleocene and that, apart from the Detarioideae WGD, paleopolyploidy occurred close to the KPB. We conclude that the early evolution of the legumes followed a complex history, in which multiple auto- and/or allopolyploidy events coincided with rapid diversification and in association with the mass extinction event at the KPB, ultimately underpinning the evolutionary success of the Leguminosae in the Cenozoic. [Allopolyploidy; Cretaceous-Paleogene (K-Pg) boundary; Fabaceae, Leguminosae; paleopolyploidy; phylogenomics; whole genome duplication events].

Reconstructing Krassilovia mongolica supports recognition of a new and unusual group of Mesozoic conifers.

Previously unrecognized anatomical features of the cone scales of the enigmatic Early Cretaceous conifer Krassilovia mongolica include the presence of transversely oriented paracytic stomata, which is unusual for all other extinct and extant conifers. Identical stomata are present on co-occurring broad, linear, multiveined leaves assigned to Podozamites harrisii, providing evidence that K. mongolica and P. harrisii are the seed cones and leaves of the same extinct plant. Phylogenetic analyses of the relationships of the reconstructed Krassilovia plant place it in an informal clade that we name the Krassilovia Clade, which also includes Swedenborgia cryptomerioides-Podozamites schenkii, and Cycadocarpidium erdmanni-Podozamites schenkii. All three of these plants have linear leaves that are relatively broad compared to most living conifers, and that are also multiveined with transversely oriented paracytic stomata. We propose that these may be general features of the Krassilovia Clade. Paracytic stomata, and other features of this new group, recall features of extant and fossil Gnetales, raising questions about the phylogenetic homogeneity of the conifer clade similar to those raised by phylogenetic analyses of molecular data.

Floral evolution and phylogeny of the Dialioideae, a diverse subfamily of tropical legumes.

PREMISE OF THE STUDY: The Dialioideae is an early diverging clade of caesalpinioid legumes containing approximately 85 species in 17 genera. Dialioideae floral morphology is highly variable and may provide clues to caesalpinioid evolution, but a well-resolved phylogeny is needed. Here, we have carried out a comprehensive morphological study of 78 Dialioideae and four outgroup species. METHODS: For all available Dialioideae DNA samples, the plastid rpS16 and trnL introns were sequenced. A combined phylogenetic analysis using the parsimony criterion was completed on a reduced taxon set for which both molecular and morphological data were available. Highly supported clades from the strict consensus tree of this analysis were then used to constrain the nodes of a second analysis on an expanded taxon set with missing molecular data for some taxa. KEY RESULTS: Several new, highly supported relationships have been discovered at the species and genus levels. The loss of the antepetalous stamen whorl was found to be a synapomorphy for most of the clade. CONCLUSIONS: A high degree of organ loss is common in the Dialioideae and often results in a bilaterally symmetrical flower. The absence of consistent morphological features in the Dialioideae, coupled with the small size of each florally diagnosed genus, suggests a lack of canalization in the floral evolution in early diverging legume lineages.

Two early eudicot fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) in northeastern Japan.

Two new fossil taxa referable to the basal eudicot grade are described from the Kamikitaba locality (ca. 89 MYBP, early Coniacian: Late Cretaceous) of the Futaba Group in Japan. These charcoalified mesofossils exhibit well-preserved three-dimensional structure and were analyzed using synchrotron-radiation X-ray microtomography to document their composition and internal structure. Cathiaria japonica sp. nov. is represented by infructescence segments that consist of an axis bearing three to four fruits. The capsular fruits are sessile and dehiscent and consist of a gynoecium subtended by a bract. No perianth parts are present. The gynoecium is monocarpellate containing two pendulous seeds. The carpel is ascidiate in the lower half and conduplicate in the upper part, and the style is deflected abaxially with a large, obliquely decurrent stigma. Pollen grains are tricolpate with a reticulate exine. The morphological features of Cathiaria are consistent with an assignment to the Buxaceae s. l. (including Didymelaceae). Archaestella verticillatus gen. et sp. nov. is represented by flowers that are small, actinomorphic, pedicellate, bisexual, semi-inferior, and multicarpellate. The floral receptacle is cup shaped with a perigynous perianth consisting of several tepals inserted around the rim. The gynoecium consists of a whorl of ten conduplicate, laterally connate but distally distinct carpels with a conspicuous dorsal bulge, including a central cavity. The styles are short, becoming recurved with a ventrally decurrent stigma. Seeds are ca. 10 per carpel, marginal, pendulous from the broad, oblique summit of the locule. Pollen grains are tricolpate with a reticulate exine pattern, suggesting a relationship to eudicots. The morphological features of Archaestella indicate a possible relationship to Trochodendraceae in the basal grade of eudicots. The fossil currently provides the earliest record of the family and documents the presence of Trochodendraceae in eastern Eurasia during the middle part of the Late Cretaceous.

The presumed ginkgophyte Umaltolepis has seed-bearing structures resembling those of Peltaspermales and Umkomasiales.

The origins of the five groups of living seed plants, including the single relictual species Ginkgo biloba, are poorly understood, in large part because of very imperfect knowledge of extinct seed plant diversity. Here we describe well-preserved material from the Early Cretaceous of Mongolia of the previously enigmatic Mesozoic seed plant reproductive structure Umaltolepis, which has been presumed to be a ginkgophyte. Abundant new material shows that Umaltolepis is a seed-bearing cupule that was borne on a stalk at the tip of a short shoot. Each cupule is umbrella-like with a central column that bears a thick, resinous, four-lobed outer covering, which opens from below. Four, pendulous, winged seeds are attached to the upper part of the column and are enclosed by the cupule. Evidence from morphology, anatomy, and field association suggests that the short shoots bore simple, elongate Pseudotorellia leaves that have similar venation and resin ducts to leaves of living GinkgoUmaltolepis seed-bearing structures are very different from those of Ginkgo but very similar to fossils described previously as Vladimaria. Umaltolepis and Vladimaria do not closely resemble the seed-bearing structures of any living or extinct plant, but are comparable in some respects to those of certain Peltaspermales and Umkomasiales (corystosperms). Vegetative similarities of the Umaltolepis plant to Ginkgo, and reproductive similarities to extinct peltasperms and corystosperms, support previous ideas that Ginkgo may be the last survivor of a once highly diverse group of extinct plants, several of which exhibited various degrees of ovule enclosure.

Palaeobotanical redux: revisiting the age of the angiosperms.

Angiosperms (flowering plants) are the most diverse of all major lineages of land plants and the dominant autotrophs in most terrestrial ecosystems. Their evolutionary and ecological appearance is therefore of considerable interest and has significant implications for understanding patterns of diversification in other lineages, including insects and other animals. More than half a century ago, influential reviews showed that while angiosperms are richly represented in sediments of Late Cretaceous and younger ages, there are no reliable records of angiosperms from pre-Cretaceous rocks. The extensive new macrofossil, mesofossil, and microfossil data that have accumulated since have confirmed and reinforced this pattern. Recently, however, molecular dating methods have raised the possibility that angiosperms may have existed much earlier, and there have been scattered reports of putative angiosperms from Triassic and Jurassic rocks. Critical assessment of these reports shows that, so far, none provide unequivocal evidence of pre-Cretaceous angiosperms. Angiosperms may ultimately be recognized from Jurassic or earlier rocks, but credible palaeobotanical evidence will require unambiguous documentation of the diagnostic structural features that separate angiosperms from other groups of extant and extinct seed plants.

An exquisitely preserved filmy fern (Hymenophyllaceae) from the Early Cretaceous of Mongolia.

PREMISE OF THE STUDY: Hymenophyllaceae ("filmy ferns") are a widely distributed group of predominantly tropical, epiphytic ferns that also include some temperate and terrestrial species. Hymenophyllaceae are one of the earliest-diverging lineages within leptosporangiate ferns, but their fossil record is sparse, most likely because of their low fossilization potential and commonly poor preservation of their delicate, membranaceous fronds. A new species of unequivocal fossil Hymenophyllaceae, Hymenophyllum iwatsukii sp. nov., is described from the Early Cretaceous of Mongolia based on abundant and exceptionally well-preserved material. METHODS: Bulk lignite samples collected from Tevshiin Govi and Tugrug localities in Mongolia, were disaggregated in water, cleaned with hydrochloric and hydrofluoric acids, washed, and dried in air. Fossils were examined and compared to material of extant Hymenophyllaceae using LM and SEM. KEY RESULTS: The fossil fern specimens are assigned to the Hymenophyllaceae based on their membranaceous laminae with marginal sori that have sessile to short-stalked sporangia with oblique, complete annuli, and trilete, tetrahedral-globose spores. Within the family, the fossil material is assigned to the extant genus Hymenophyllum on the basis of bivalvate indusia and short, included receptacles. CONCLUSIONS: Hymenophyllum iwatsukii was likely an epiphyte based on the sedimentary environment in which the fossils are preserved, the associated fossil flora, and the growth habit of extant species of Hymenophyllum. The new fossil species underlines the extent to which morphological characters in Hymenophyllum have been conserved despite significant tectonic, climatic, ecological, and floristic changes since the Early Cretaceous.

Early Cretaceous Umkomasia from Mongolia: implications for homology of corystosperm cupules.

Corystosperms, a key extinct group of Late Permian to Early Cretaceous plants, are important for understanding seed plant phylogeny, including the evolution of the angiosperm carpel and anatropous bitegmic ovule. Here, we describe a new species of corystosperm seed-bearing organ, Umkomasia mongolica sp. nov., based on hundreds of three-dimensionally preserved mesofossils from the Early Cretaceous of Mongolia. Individual seed-bearing units of U. mongolica consist of a bract subtending an axis that bifurcates, with each fork (cupule stalk) bearing a cupule near the tip. Each cupule is formed by the strongly reflexed cupule stalk and two lateral flaps that partially enclose an erect seed. The seed is borne at, or close to, the tip of the reflexed cupule stalk, with the micropyle oriented towards the stalk base. The corystosperm cupule is generally interpreted as a modified leaf that bears a seed on its abaxial surface. However, U. mongolica suggests that an earlier interpretation, in which the seed is borne directly on an axis (shoot), is equally likely. The 'axial' interpretation suggests a possible relationship of corystosperms to Ginkgo. It also suggests that the cupules of corystosperms may be less distinct from those of Caytonia than has previously been supposed.

Pinaceae-like reproductive morphology in Schizolepidopsis canicularis sp. nov. from the Early Cretaceous (Aptian-Albian) of Mongolia.

PREMISE OF THE STUDY: Seed cone scales assigned to the genus Schizolepidopsis are widespread in Late Triassic to Cretaceous Eurasian deposits. They have been linked to the conifer family Pinaceae based on associated vegetative remains, but their exact affinities are uncertain. Recently discovered material from the Early Cretaceous of Mongolia reveals important new information concerning Schizolepidopsis cone scales and seeds, and provides support for a relationship between the genus and extant Pinaceae. METHODS: Specimens were collected from Early Cretaceous (probable Aptian-Albian) lignite deposits in central Mongolia. Lignite samples were disaggregated, cleaned in hydrofluoric acid, and washed in water. Specimens were selected for further study using light and electron microscopy. KEY RESULTS: Schizolepidopsis canicularis seed cones consist of loosely arranged, bilobed ovulate scales subtended by a small bract. A single inverted seed with an elongate micropyle is borne on each lobe of the ovulate scale. Each seed has a wing formed by the separation of the adaxial surface of the ovulate scale. CONCLUSIONS: Schizolepidopsis canicularis produced winged seeds that formed in a manner that is unique to Pinaceae among extant conifers. We do not definitively place this species in Pinaceae pending more complete information concerning its pollen cones and vegetative remains. Nevertheless, this material suggests that Schizolepidopsis may be important for understanding the early evolution of Pinaceae, and may potentially help reconcile the appearance of the family in the fossil record with results based on phylogenetic analyses of molecular data.

Glandulocalyx upatoiensis, a fossil flower of Ericales (Actinidiaceae/Clethraceae) from the Late Cretaceous (Santonian) of Georgia, USA.

BACKGROUND AND AIMS: Ericales are a major group of extant asterid angiosperms that are well represented in the Late Cretaceous fossil record, mainly by flowers, fruits and seeds. Exceptionally well preserved fossil flowers, here described as Glandulocalyx upatoiensis gen. & sp. nov., from the Santonian of Georgia, USA, yield new detailed evidence of floral structure in one of these early members of Ericales and provide a secure basis for comparison with extant taxa. METHODS: The floral structure of several fossil specimens was studied by scanning electron microscopy (SEM), light microscopy of microtome thin sections and synchrotron-radiation X-ray tomographic microscopy (SRXTM). For direct comparisons with flowers of extant Ericales, selected floral features of Actinidiaceae and Clethraceae were studied with SEM. KEY RESULTS: Flowers of G. upatoiensis have five sepals with quincuncial aestivation, five free petals with quincuncial aestivation, 20-28 stamens arranged in a single series, extrorse anther orientation in the bud, ventral anther attachment and a tricarpellate, syncarpous ovary with three free styles and numerous small ovules on axile, protruding-diffuse and pendant placentae. The calyx is characterized by a conspicuous indumentum of large, densely arranged, multicellular and possibly glandular trichomes. CONCLUSIONS: Comparison with extant taxa provides clear evidence for a relationship with core Ericales comprised of the extant families Actinidiaceae, Roridulaceae, Sarraceniaceae, Clethraceae, Cyrillaceae and Ericaceae. Within this group, the most marked similarities are with extant Actinidiaceae and, to a lesser degree, with Clethraceae. More detailed analyses of the relationships of Glandulocalyx and other Ericales from the Late Cretaceous will require an improved understanding of the morphological features that diagnose particular extant groups defined on the basis of molecular data.