Early Angiosperm Diversification Research Articles

Cretaceous chloranthoids: early prominence, extinct diversity and missing links.

The Chloranthaceae comprise four extant genera (Hedyosmum, Ascarina, Chloranthus and Sarcandra), all with simple flowers. Molecular phylogenetics indicates that the Chloranthaceae diverged very early in angiosperm evolution, although how they are related to eudicots, magnoliids, monocots and Ceratophyllum is uncertain. Fossil pollen similar to that of Ascarina and Hedyosmum has long been recognized in the Early Cretaceous, but over the last four decades evidence of extinct Chloranthaceae based on other types of fossils has expanded dramatically and contributes significantly to understanding the evolution of the family. Studies of fossils from the Cretaceous, especially mesofossils of Early Cretaceous age from Portugal and eastern North America, recognized diverse flowers, fruits, seeds, staminate inflorescences and stamens of extinct chloranthoids. These early chloranthoids include forms related to extant Hedyosmum and also to the Ascarina, Chloranthus and Sarcandra clade. In the Late Cretaceous there are several occurrences of distinctive fossil androecia related to extant Chloranthus. The rich and still expanding Cretaceous record of Chloranthaceae contrasts with a very sparse Cenozoic record, emphasizing that the four extant genera are likely to be relictual, although speciation within the genera might have occurred in relatively recent times. In this study, we describe three new genera of Early Cretaceous chloranthoids and summarize current knowledge on the extinct diversity of the group. The evolutionary lineage that includes extant Chloranthaceae is diverse and abundantly represented in Early Cretaceous mesofossil floras that provide some of the earliest evidence of angiosperm reproductive structures. Extinct chloranthoids, some of which are clearly in the Chloranthaceae crown group, fill some of the morphological gaps that currently separate the extant genera, help to illuminate how some of the unusual features of extant Chloranthaceae evolved and suggest that Chloranthaceae are of disproportionate importance for a more refined understanding of ecology and phylogeny of early angiosperm diversification.

Expanding the diversity of conifer xyloflora from Early Cretaceous Crato Fossil Lagerstätte, Brazil

Remains of gymnosperms are the most abundant plant macro-fossils in the outcrops of a fossil lagerstätte preserved in lacustrine limestones in the likely lower Aptian Crato Formation of the Araripe Basin in NE Brazil. However, the systematics of most fossil-taxa are mainly based on foliage and reproductive structures, whereas wood anatomy has rarely been used to study fossil plant diversity, despite the abundance of wood fragments. Here we describe a new fossil gymnosperm taxon based on anatomical characters of a well-preserved specimen from this lithostratigraphic unit. The new fossil-genus and fossil-species Cratoxylon placidoi gen. nov. et sp. nov. are established using characters of the secondary xylem and the bark, features that are also crucial for their affiliation into conifers. This finding reinforces the already known remarkable preservation potential of organisms in this konservat lagerstätte, since bark tissues are rarely preserved in the fossil record of Mesozoic gymnosperms. The results reveal the great potential of fossil woods for studying diversity of the Crato Formation flora and thus contribute to expand our knowledge on fossil vegetation in equatorial Gondwana during the early diversification of angiosperms.

Patterns of variation in fleshy diaspore size and abundance from Late Triassic-Oligocene.

Vertebrate-mediated seed dispersal is a common attribute of many living plants, and variation in the size and abundance of fleshy diaspores is influenced by regional climate and by the nature of vertebrate seed dispersers among present-day floras. However, potential drivers of large-scale variation in the abundance and size distributions of fleshy diaspores through geological time, and the importance of geographic variation, are incompletely known. This knowledge gap is important because fleshy diaspores are a key mechanism of energy transfer from photosynthesis to animals and may in part explain the diversification of major groups within birds and mammals. Various hypotheses have been proposed to explain variation in the abundance and size distribution of fleshy diaspores through time, including plant-frugivore co-evolution, angiosperm diversification, and changes in vegetational structure and climate. We present a new data set of more than 800 georeferenced fossil diaspore occurrences spanning the Triassic-Oligocene, across low to mid- to high palaeolatitudes. We use this to quantify patterns of long-term change in fleshy diaspores, examining the timing and geographical context of important shifts as a test of the potential evolutionary and climatic explanations. We find that the fleshy fruit sizes of angiosperms increased for much of the Cretaceous, during the early diversification of angiosperms from herbaceous ancestors with small fruits. Nevertheless, this did not cause a substantial net change in the fleshy diaspore size distributions across seed plants, because gymnosperms had achieved a similar size distribution by at least the Late Triassic. Furthermore, gymnosperm-dominated Mesozoic ecosystems were mostly open, and harboured low proportions of specialised frugivores until the latest Cretaceous, suggesting that changes in vegetation structure and plant-frugivore co-evolution were probably not important drivers of fleshy diaspore size distributions over long timescales. Instead, fleshy diaspore size distributions may be largely constrained by physical or life-history limits that are shared among groups and diversify as a plant group expands into different growth forms/sizes, habitats, and climate regimes. Mesozoic gymnosperm floras had a low abundance of fleshy diaspores (<50% fleshy diaspore taxa), that was surpassed by some low-latitude angiosperm floras in the Cretaceous. Eocene angiosperm floras show a mid- to high latitude peak in fleshy fruit abundance, with very high proportions of fleshy fruits that even exceed those seen at low latitudes both in the Eocene and today. Mid- to high latitude proportions of fleshy fruits declined substantially over the Eocene-Oligocene transition, resulting in a shift to more modern-like geographic distributions with the highest proportion of fleshy fruits occurring in low-latitude tropical assemblages. This shift was coincident with global cooling and the onset of Southern Hemisphere glaciation, suggesting that rapid cooling at mid- and high latitudes caused a decrease in availability of the climate conditions most favourable for fleshy fruits in angiosperms. Future research could be focused on examining the environmental niches of modern fleshy fruits, and the potential effects of climate change on fleshy fruit and frugivore diversity.

Multipartite Flowers with a Distinct Floral Cup and Multiovulate Carpels: An Early Cretaceous Angiosperm of Probable Lauralean Relationship

Premise of research. Typically, the small coalified mesofossil flowers known from the Early Cretaceous have character combinations that are unknown among extant angiosperms, highlighting that many extinct lineages, which will be important for understanding the early diversification of angiosperms, are currently unrecognized. The fossils studied here provide a further example of an early angiosperm flower with an unusual combination of features of extant Laurales and other magnoliids.Methodology. Mesofossils were extracted from the sediments, cleaned using standard methods, and investigated using scanning electron microscopy and synchrotron radiation X-ray tomographic microscopy. Comparisons with extant and fossil taxa, and a phylogenetic assessment using the existing Doyle and Endress data set for extant angiosperms, were used to assess potential relationships.Pivotal results. Racheliflora is named as a new Early Cretaceous flower based on floral buds with an obconical floral cup. The perianth has about six whorls, each of four tepals. Tepals borne on the outside of the floral cup are bract-like, while inner tepals are more petallike and borne on the rim of the floral cup. The androecium comprises two whorls of four bulky, partly laminar stamens that are also borne on the rim of the floral cup. The gynoecium is apocarpous with three free carpels, each of which contains many ovules borne along two ventral placentae.Conclusions. Racheliflora is most closely related to extant magnoliids but possesses a combination of characters that is unknown among extant taxa. It has several carpels borne in a distinct floral cup, as in pluricarpellate members of Laurales, but the multiovulate carpels and bulky, laminar stamens are unknown in Laurales and more like features seen in other groups of magnoliids.

Chloranthus genome provides insights into the early diversification of angiosperms

Chloranthales remain the last major mesangiosperm lineage without a nuclear genome assembly. We therefore assemble a high-quality chromosome-level genome of Chloranthus spicatus to resolve enigmatic evolutionary relationships, as well as explore patterns of genome evolution among the major lineages of mesangiosperms (eudicots, monocots, magnoliids, Chloranthales, and Ceratophyllales). We find that synteny is highly conserved between genomic regions of Amborella, Vitis, and Chloranthus. We identify an ancient single whole-genome duplication (WGD) (κ) prior to the divergence of extant Chloranthales. Phylogenetic inference shows Chloranthales as sister to magnoliids. Furthermore, our analyses indicate that ancient hybridization may account for the incongruent phylogenetic placement of Chloranthales + magnoliids relative to monocots and eudicots in nuclear and chloroplast trees. Long genes and long introns are found to be prevalent in both Chloranthales and magnoliids compared to other angiosperms. Overall, our findings provide an improved context for understanding mesangiosperm relationships and evolution and contribute a valuable genomic resource for future investigations.

Early Cretaceous mealybug herbivory on a laurel highlights the deep-time history of angiosperm-scale insect associations.

Insect fluid-feeding on fossil vascular plants is an inconspicuous and underappreciated mode of herbivory that can provide novel data on the evolution of deep-time ecological associations and indicate the host-plant preferences of ancient insect herbivores. Previous fossil studies have documented piercing-and-sucking herbivory but often are unable to identify culprit insect taxa. One line of evidence are punctures and scale-insect impression marks made by piercing-and-sucking insects that occasionally provide clues to the systematic identities and relationships of particular insect herbivores. We report here the earliest occurrences of piercing and sucking on early angiosperms as evidenced by scale insect covers, impression marks, punctures and body fossils - notably a mealybug - from the Lower Cretaceous Rose Creek Flora of the Dakota Formation (c. 103Ma), in southeastern Nebraska, USA. The mealybug, two other scale insect taxa, and several distinctive damage types on laurel leaves and seed-plant stems at Rose Creek document a diverse guild of piercing-and-sucking insects on early angiosperms. The discovery of an Early Cretaceous female mealybug indicates an early herbivorous association with a laurel host. These data provide direct evidence for co-associations and possible coevolution of scale insects and their plant hosts during early angiosperm diversification.

Mitochondrial genes from 18 angiosperms fill sampling gaps for phylogenomic inferences of the early diversification of flowering plants

AbstractThe early diversification of angiosperms is thought to have been a rapid process, which may complicate phylogenetic analyses of early angiosperm relationships. Plastid and nuclear phylogenomic studies have raised several conflicting hypotheses regarding overall angiosperm phylogeny, but mitochondrial genomes have been largely ignored as a relevant source of information. Here we sequenced mitochondrial genomes from 18 angiosperms to fill taxon‐sampling gaps in Austrobaileyales, magnoliids, Chloranthales, Ceratophyllales, and major lineages of eudicots and monocots. We assembled a data matrix of 38 mitochondrial genes from 107 taxa to assess how well mitochondrial genomic data address current uncertainties in angiosperm relationships. Although we recovered conflicting phylogenies based on different data sets and analytical methods, we also observed congruence regarding deep relationships of several major angiosperm lineages: Chloranthales were always inferred to be the sister group of Ceratophyllales, Austrobaileyales to mesangiosperms, and the unplaced Dilleniales was consistently resolved as the sister to superasterids. Substitutional saturation, GC compositional heterogeneity, and codon‐usage bias are possible reasons for the noise/conflict that may impact phylogenetic reconstruction; and angiosperm mitochondrial genes may not be substantially affected by these factors. The third codon positions of the mitochondrial genes appear to contain more parsimony‐informative sites than the first and second codon positions, and therefore produced better resolved phylogenetic relationships with generally strong support. The relationships among these major lineages remain incompletely resolved, perhaps as a result of the rapidity of early radiations. Nevertheless, data from mitochondrial genomes provide additional evidence and alternative hypotheses for exploring the early evolution and diversification of the angiosperms.

Palynological analysis of a Lower Cretaceous subsurface succession from the south flank of the Golfo San Jorge Basin, Argentina

Abundant and well-preserved palynological assemblages recovered from the Las Heras Group and Pozo D-129 Formation in the YPF.SC.PL x-2 (Puesto Ludden) are analyzed. This well includes the most complete Lower Cretaceous succession along the south flank of the Golfo San Gorge Basin. The palynofloras comprise fifty spore species, twenty-eight pollen taxa (including two angiosperm pollen taxa) and four algae. A late Valanginian–Hauterivian age is suggested for the Las Heras Group based mainly on the presence of Cyclusphaera psilata, Foraminisporis variornatus and Celyphus rallus and the absence of angiosperm pollen. These assemblages can be correlated with the Interulobites-Foraminisporis Zone (upper Valanginian–Hauterivian) of the Austral Basin. On the other hand, a Barremian-early Aptian age for the palynofloras from the Pozo D-129 Formation is suggested based on the sparse angiosperm pollen grains identified (Clavatipollenites sp. and Afropollis sp.) and it is correlated with the Antulsporites-Clavatipollenites Zone (Aptian) of the Austral Basin. These palynofloras from the Pozo D-129 Formation are representative of the initial late Barremian-Aptian phase of the early angiosperm diversification in central and southern Argentinean basins.

Early angiosperm diversification in the Albian of southeast Australia: implications for flowering plant radiation across eastern Gondwana

This study provides the first record of the high diversity and abundance of Victoria's earliest angiosperms from outcrops in the non-marine upper Eumeralla Formation of the Otway Basin. The biostratigraphic schemes established for the Albian of Australia are re-evaluated using more reliable and widespread index species, resulting in the construction of a high-resolution Albian biostratigraphy in the Otway Basin. New localities in the uppermost outcrop of the Eumerella Formation contain spore–pollen assemblages that cannot be placed in the existing scheme and a new Upper Phimopollenites pannosus Subzone is recognised. The correlation of the P. pannosus Zone to the geochronological timescale was re-assessed and shows that it is 103–101.51Ma, giving a late Albian age. In contrast to previous studies that record low diversity angiosperm assemblages in the Albian, this study identifies twenty-three angiosperm species, including one new species, Tricolpites tortuous. The high diversity and abundance of angiosperm pollen in the Otway Basin provides further evidence that angiosperms probably migrated into eastern Gondwana via South America and Antarctica.

The Amborella vacuolar processing enzyme family.

Most vacuolar proteins are synthesized on rough endoplasmic reticulum as proprotein precursors and then transported to the vacuoles, where they are converted into their respective mature forms by vacuolar processing enzymes (VPEs). In the case of the seed storage proteins, this process is of major importance, as it conditions the establishment of vigorous seedlings. Toward the goal of identifying proteome signatures that could be associated with the origin and early diversification of angiosperms, we previously characterized the 11S-legumin-type seed storage proteins from Amborella trichopoda, a rainforest shrub endemic to New Caledonia that is also the probable sister to all other angiosperms (Amborella Genome Project, 2013). In the present study, proteomic and genomic approaches were used to characterize the VPE family in this species. Three genes were found to encode VPEs in the Amborella's genome. Phylogenetic analyses showed that the Amborella sequences grouped within two major clades of angiosperm VPEs, indicating that the duplication that generated the ancestors of these clades occurred before the most recent common ancestor of living angiosperms. A further important duplication within the VPE family appears to have occurred in common ancestor of the core eudicots, while many more recent duplications have also occurred in specific taxa, including both Arabidopsis thaliana and Amborella. An analysis of natural genetic variation for each of the three Amborella VPE genes revealed the absence of selective forces acting on intronic and exonic single-nucleotide polymorphisms among several natural Amborella populations in New Caledonia.

Montsechia, an ancient aquatic angiosperm

The early diversification of angiosperms in diverse ecological niches is poorly understood. Some have proposed an origin in a darkened forest habitat and others an open aquatic or near aquatic habitat. The research presented here centers on Montsechia vidalii, first recovered from lithographic limestone deposits in the Pyrenees of Spain more than 100 y ago. This fossil material has been poorly understood and misinterpreted in the past. Now, based upon the study of more than 1,000 carefully prepared specimens, a detailed analysis of Montsechia is presented. The morphology and anatomy of the plant, including aspects of its reproduction, suggest that Montsechia is sister to Ceratophyllum (whenever cladistic analyses are made with or without a backbone). Montsechia was an aquatic angiosperm living and reproducing below the surface of the water, similar to Ceratophyllum. Montsechia is Barremian in age, raising questions about the very early divergence of the Ceratophyllum clade compared with its position as sister to eudicots in many cladistic analyses. Lower Cretaceous aquatic angiosperms, such as Archaefructus and Montsechia, open the possibility that aquatic plants were locally common at a very early stage of angiosperm evolution and that aquatic habitats may have played a major role in the diversification of some early angiosperm lineages.

Proto-South-East Asia as a trigger of early angiosperm diversification

Darwin described as an ‘abominable mystery’ the abrupt origin of angiosperms in the mid-Cretaceous and the high diversification rates in their early history. The father of evolutionary theory could not fathom this rapid diversification and rather invoked that ‘there was during long ages a small isolated continent in the S. hemisphere, which served as the birthplace of the higher plants’. In this essay, we comment on the spatial origin of angiosperms, but focus primarily on understanding the abiotic factors that promoted the early diversification of angiosperms by reviewing palaeobotanical, palaeogeographical, phylogenetics and biogeographical evidence. We argue that islands located in the region today occupied by South-East Asia played a major role in angiosperm diversification during the Late Jurassic and Early Cretaceous. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333.

High-precision U–Pb zircon age from the Anfiteatro de Ticó Formation: Implications for the timing of the early angiosperm diversification in Patagonia

The Baqueró Group is one of the most relevant units regarding the study of the early diversification of angiosperms in South America. Whereas the age of the upper part of the Group, namely the Punta del Barco Formation, has been recently dated at 114.67 ± 0.18 Ma, the rest of the unit still lacks precise dating. In this contribution a CA-TIMS U–Pb zircon age of 118.23 ± 0.09 Ma for a tuff interlayered with fossiliferous rocks of the Anfiteatro de Ticó Formation (lower part of the Baqueró Group) is reported. This age constrains the duration of deposition of the Baqueró Group to approximately 4 Ma and provides new evidence for the age interpretation of the previously described angiosperm flora and associated pollen assemblages from this unit, until now interpreted as early Aptian or possibly Barremian in age. The Aptian age of the Baqueró Group allows a better comparison between the paleofloras from this southernmost region.

Palynological composition of a Lower Cretaceous South American tropical sequence: Climatic implications and diversity comparisons with other latitudes

Reconstruction of floristic patterns during the early diversification of angiosperms is impeded by the scarce fossil record, especially in tropical latitudes. Here we collected quantitative palynological data from a stratigraphic sequence in tropical South America to provide floristic and climatic insights into such tropical environments during the Early Cretaceous. We reconstructed the floristic composition of an Aptian-Albian tropical sequence from central Colombia using quantitative palynology (rarefied species richness and abundance) and used it to infer its predominant climatic conditions. Additionally, we compared our results with available quantitative data from three other sequences encompassing 70 floristic assemblages to determine latitudinal diversity patterns. Abundance of humidity indicators was higher than that of aridity indicators (61% vs. 10%). Additionally, we found an angiosperm latitudinal diversity gradient (LDG) for the Aptian, but not for the Albian, and an inverted LDG of the overall diversity for the Albian. Angiosperm species turnover during the Albian, however, was higher in humid tropics. There were humid climates in northwestern South America during the Aptian-Albian interval contrary to the widespread aridity expected for the tropical belt. The Albian inverted overall LDG is produced by a faster increase in per-sample angiosperm and pteridophyte diversity in temperate latitudes. However, humid tropical sequences had higher rates of floristic turnover suggesting a higher degree of morphological variation than in temperate regions.

328 Floristic reconstruction of two Lower Cretaceous sections from Peru during the period of early angiosperm diversification and their climatic implications

328 Floristic reconstruction of two Lower Cretaceous sections from Peru during the period of early angiosperm diversification and their climatic implications

Diversity in obscurity: fossil flowers and the early history of angiosperms

In the second half of the nineteenth century, pioneering discoveries of rich assemblages of fossil plants from the Cretaceous resulted in considerable interest in the first appearance of angiosperms in the geological record. Darwin's famous comment, which labelled the 'rapid development' of angiosperms an 'abominable mystery', dates from this time. Darwin and his contemporaries were puzzled by the relatively late, seemingly sudden and geographically widespread appearance of modern-looking angiosperms in Late Cretaceous floras. Today, the early diversification of angiosperms seems much less 'rapid'. Angiosperms were clearly present in the Early Cretaceous, 20-30 Myr before they attained the level of ecological dominance reflected in some mid-Cretaceous floras, and angiosperm leaves and pollen show a distinct pattern of steadily increasing diversity and complexity through this interval. Early angiosperm fossil flowers show a similar orderly diversification and also provide detailed insights into the changing reproductive biology and phylogenetic diversity of angiosperms from the Early Cretaceous. In addition, newly discovered fossil flowers indicate considerable, previously unrecognized, cryptic diversity among the earliest angiosperms known from the fossil record. Lineages that today have an herbaceous or shrubby habit were well represented. Monocotyledons, which have previously been difficult to recognize among assemblages of early fossil angiosperms, were also diverse and prominent in many Early Cretaceous ecosystems.

Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification

Angiosperm evolution transformed global ecology, and much of this impact derives from the unrivalled vegetative productivity of dominant angiosperm clades. However, the origins of high photosynthetic capacity in angiosperms remain unknown. In this study, we describe the steep trajectory of leaf vein density (D(v)) evolution in angiosperms, and predict that this leaf plumbing innovation enabled a major shift in the capacity of leaves to assimilate CO(2). Reconstructing leaf vein evolution from an examination of 504 angiosperm species we found a rapid three- to fourfold increase in D(v) occurred during the early evolution of angiosperms. We demonstrate how this major shift in leaf vein architecture potentially allowed the maximum photosynthetic capacity in angiosperms to rise above competing groups 140-100 Ma. Our data suggest that early terrestrial angiosperms produced leaves with low photosynthetic rates, but that subsequent angiosperm success is linked to a surge in photosynthetic capacity during their early diversification.

Evolution of Plant MADS Box Transcription Factors: Evidence for Shifts in Selection Associated with Early Angiosperm Diversification and Concerted Gene Duplications

Phylogenomic analyses show that gene and genome duplication events have led to the diversification of transcription factor gene families throughout the evolutionary history of land plants and that gene duplications have played an important role in shaping regulatory networks influencing key phenotypic characters including floral development and flowering time. A molecular evolutionary investigation of the mode and tempo of selection acting on the angiosperm MADS box AP1/SQUA, AP3/PI, AG/AGL11, and SEP gene subfamilies revealed site-specific patterns of shifting evolutionary constraint throughout angiosperm history. Specific positions in the four canonical MADS box gene regions, especially K domains and C-terminal regions of all four of these MADS box gene subfamilies exhibited clade-specific shifts in selective constraint following concerted duplication events. Moreover, the frequency of site-specific shifts in constraint was correlated with gene duplications and early angiosperm diversification. We hypothesize that coevolution among interacting MADS box proteins may be responsible for simultaneous increases in the ratio of nonsynonymous to synonymous substitutions (d(N)/d(S) = omega) early in angiosperm history and following concerted duplication events.

High-precision 40Ar/ 39Ar age for the Jehol Biota

Abundant fossils of the terrestrial Jehol Biota, including plants, insects, dinosaurs, birds, mammals and freshwater invertebrates, were discovered from the Yixian Formation and the overlying Jiufotang Formation in Inner Mongolia, Hebei Province and Liaoning Province, northeastern China. Because of the exceptional preservation of fossils, the Jehol Biota is one of the most important Mesozoic lagerstätten and is referred to as a “Mesozoic Pompeii”. The Jehol Biota has provided a rare opportunity to address questions about the origin of birds, the evolution of feathers and flight, the early diversification of angiosperms and the timing of placental mammal radiation. Six tuff samples and two basalt samples collected from the Tuchengzi, the Yixian and the Jiufotang formations near the classic outcrops in western Liaoning, NE China yielded high-precision 40Ar/ 39Ar ages. We obtain an age of 129.7 ± 0.5 Ma for a basaltic lava from the bottom of the Yixian Formation and an age of 122.1 ± 0.3 Ma for a tuff from the lowermost part of the overlying Jiufotang Formation. Our age results provide an age calibration of the whole Yixian Formation and show that the whole formation was deposited entirely within Early Cretaceous time over an interval of ~ 7 Ma.

Hydatellaceae are water lilies with gymnospermous tendencies

The flowering plant family Hydatellaceae was recently discovered to be allied to the ancient angiosperm lineage Nymphaeales (water lilies). Because of its critical phylogenetic position, members of the Hydatellaceae have the potential to provide insights into the origin and early diversification of angiosperms. Here I report that Hydatella expresses several rare embryological features that, in combination, are found only in members of the Nymphaeales. At maturity, the female gametophyte is four-celled, four-nucleate and will produce a diploid endosperm, as is characteristic of most early divergent angiosperm lineages. As with all members of the Nymphaeales, endosperm in Hydatella is minimally developed and perisperm is the major embryo-nourishing tissue within the seed. Remarkably, Hydatella exhibits a maternal seed-provisioning strategy that is unique among flowering plants, but common to all gymnosperms: pre-fertilization allocation of nutrients to the embryo-nourishing tissue. This exceptional case of pre-fertilization maternal provisioning of a seed in Hydatella may well be an apomorphic feature of Hydatellaceae alone but, given the newly discovered phylogenetic position of this family, potentially represents a plesiomorphic and transitional condition associated with the origin of flowering plants from gymnospermous ancestors.