Fossil evidence for sporeling development of a Mesozoic osmundaceous fern.

PREMISE: An anatomically preserved fossil fern sporeling has been discovered in a Lower Cretaceous marine concretion from Vancouver Island, British Columbia, Canada, providing an opportunity to characterize rhizome growth from an extinct species. METHODS: The specimen was studied from serial transverse sections prepared by the cellulose acetate peel technique. RESULTS: The rhizome ranges from ~0.7 to 1.1 mm in diameter, has a sclerenchymatous pith, a stele that attains a dictyoxylic architecture, and sclerenchymatous outer cortex, features that are characteristic of osmundaceous rhizomes. Cauline xylem forms a medullated protostele or solenostele at some levels, but is dissected into discrete xylem bundles at others. Fronds diverge in a helical phyllotaxis, range up to 1.1 mm in greatest dimension, and have a C-shaped trace and outer cortex of sclerotic cells. Inside the sclerenchyma of the petioles are two lateral sclerotic strands and a sclerotic bundle adaxial to the trace. Together, these characters reveal the occurrence of a new species, Todea minutacaulis and provide evidence for developmental changes that occur in the rhizome as the sporeling increased in size. CONCLUSIONS: Small size of the specimen, medullated protostelic-dictyoxylic solenostelar vascular architecture, and incompletely sclerified cells apically reveal that osmundaceous sporeling development has remained constant since at least the Early Cretaceous. Together with Todea tidwellii and Osmunda vancouverensis that also are present in the Apple Bay flora, this sporeling documents the occurrence of a multispecies assemblage of osmundaceous ferns and demonstrates that the genus Todea was diversifying rapidly by the Early Cretaceous.

A novel cupulate seed plant, Xadzigacalix quatsinoensis gen. et sp. nov., provides new insight into the Mesozoic radiation of gymnosperms.

PREMISE: Anatomically preserved evidence for a novel clade of gymnosperms emphasizes diversity of seed plants immediately prior to the appearance of angiosperm fossils in the paleontological record. METHODS: Cupulate seeds from the Early Cretaceous Apple Bay locality (Vancouver Island) are described from serial cellulose acetate peels and three-dimensional reconstruction. Phylogenetic context is assessed through the comparative analysis of gymnosperm seed producing fructifications and maximum parsimony analysis of a revised morphological data set for seed plant phylogeny. RESULTS: Xadzigacalix quatsinoensis gen. et sp. nov. is characterized by an orthotropous ovule with an elongated micropyle and complex integument, enclosed within a radial cupule. The micropylar canal is elongated; and the nucellus extends into the micropyle to seal the post pollination ovule. Except at the apex of the micropyle, the seed is completely enclosed by a parenchymatous cupule with ca. 20 axially elongated secretory ducts. The cupulate seed is produced upon a triangular woody stele, consisting of a parenchymatous pith surrounded by radially aligned tracheids. The stele produces three short terete traces that terminate within the base of the cupule as transfusion tissue at the seed chalaza. CONCLUSIONS: Organography, vascularization, nature of the integument and nucellus, and configuration of the micropylar canal distinguish Xadzigacalix quatsinoensis from all other gymnosperm clades. Cladistic analyses suggest the new plant may have affinities with gnetophytes or angiosperms. These results are complemented with a critical re-evaluation of ovulate structures for Mesozoic gymnosperms, providing new insight into plant diversity immediately antecedent to the explosive diversification of flowering plants.

Cynodontium luthii sp. nov.: a permineralized moss gametophyte from the Late Cretaceous of the North Slope of Alaska.

PREMISE: Mosses are a major component of Arctic vegetation today, with >500 species known to date. However, the origins of the Arctic moss flora are poorly documented in the fossil record, especially prior to the Pliocene. Here, we present the first anatomically preserved pre-Cenozoic Arctic moss and discuss how the unique biology of bryophytes has facilitated their success in polar environments over geologic time. METHODS: A permineralized fossil moss gametophyte within a block of Late Cretaceous terrestrial limestone, collected along the Colville River on the North Slope of Alaska, was studied in serial sections prepared using the cellulose acetate peel technique. RESULTS: The moss gametophyte is branched and has leaves with a broad base, narrow blade, and excurrent costa. We describe this fossil as Cynodontium luthii sp. nov., an extinct species of a genus that is known from the High Arctic today. Cynodontium luthii is the oldest evidence of the family Rhabdoweisiaceae (by ≥18 Ma) and reveals that genera of haplolepideous mosses known in the extant Arctic flora also lived in high-latitude temperate deciduous forests during the Late Cretaceous. CONCLUSIONS: The occurrence of C. luthii in Cretaceous sediments, together with a rich Pliocene-to-Holocene fossil record of extant moss genera in the High Arctic, suggests that some moss lineages have exploited their poikilohydric, cold- and desiccation-tolerant physiology to live in the region when it experienced both temperate and freezing climates.

Fossil evidence for Paleocene diversification of Araceae: Bognerospadix gen. nov. and Orontiophyllum grandifolium comb. nov.

PREMISE: Nearly 200 araceous leaves and two spadices have been identified among Paleocene fossils from the Blindman River locality near Blackfalds, Alberta, Canada. Although not found in attachment, these probably represent parts of the same extinct plant species. METHODS: Specimens were studied using light microscopy. Phylogenetic analyses using a morphological matrix of living and fossil Araceae were performed using TNT version 1.5 to help establish relationships of the fossil leaves and spadices within Araceae and to each other. RESULTS: Leaves are simple with a broad petiole, entire margin, and elliptic to ovate or oblong blade with an acute to slightly rounded apex. A multi-veined midrib extends into the basal region of the blade. Parallelodromous primary veins of two orders diverge at acute angles, converging with a submarginal vein or at the apex. Transverse veins are opposite percurrent, producing rectangular to polygonal areoles. Higher-order veins are mixed opposite/alternate. Spadices are cylindrical, with helically arranged, bisexual, perigoniate flowers, each with six free tepals and a protruding style. Fruits are trilocular, with axile placentation and one seed per locule. CONCLUSIONS: Leaves are assignable to the fossil genus Orontiophyllum J. Kvacek & S.Y. Sm. as O. grandifolium comb. nov. Spadices are described as Bognerospadix speirsiae gen. et sp. nov. Leaves and spadices each conform to an early-diverging lineage of Araceae, increasing the known diversity of Proto-Araceae (viz., subfamilies Gymnostachydoideae and Orontioideae). Together, they provide strong evidence for extinct Proto-Araceae with novel combinations of characters shortly after the Cretaceous-Paleogene floral transition.

Diversification of crown group Araucaria: the role of Araucaria famii sp. nov. in the mid-Cretaceous (Campanian) radiation of Araucariaceae in the Northern Hemisphere.

PREMISE: Exceptional anatomical preservation of a fossil araucarian seed cone from a marine carbonate concretion from Vancouver Island, British Columbia, Canada provides unusually complete evidence for cone structure including seeds, megagametophytes, microgametophytes, and embryos of an Upper Cretaceous (Campanian) species of Araucaria, providing important new insights into the structure and relationships of Cretaceous Northern Hemisphere Araucariaceae. METHODS: The cone was studied from serial thin sections prepared by the coal ball peel technique. Phylogenetic analysis using a modified morphological matrix with both discrete and continuous characters was performed using TNT version 1.5. RESULTS: The nearly spherical cone, 6 × 6 cm in diameter, has helically arranged cone-scale complexes, consisting of a large bract with an upturned tip and a small, fleshy ovuliferous scale. Vascularization of the cone-scale complex is single at its origin. Widely winged bracts, with a bulging base, contain numerous vascular bundles, interspersed with transfusion tissue, and a large number of resin canals. Seeds are ovoid, 1.2 cm long, 1.2 cm in diameter. Nucellus is free from the integument, except at its base, with a convoluted apex, containing possible pollen tubes. Megagametophytes and mature cellular embryos occur in several seeds. CONCLUSIONS: This small cone with attached, imbricate leaves, wide bracts, and unusually large seeds, most closely resembles those of Araucaria Section Eutacta. Width and continuity of secondary xylem in the cone axis, and intact cone-scale complexes indicate that this cone probably did not disarticulate readily at maturity. When added to a modified, previously published phylogenetic analysis, Araucaria famii sp. nov. enhances our understanding of the Cretaceous radiation of Northern Hemisphere Araucaria Section Eutacta.

Evolutionary diversification of taiwanioid conifers: evidence from a new Upper Cretaceous seed cone from Hokkaido, Japan.

A single cylindrical seed cone 2 cm long, 1.1 cm wide has been found preserved in a calcium carbonate marine concretion from the Hakobuchi Formation (late Campanian-early Maastrichtian) of Hobetsu, Hokkaido, Japan. The cone, attached to a bent peduncle lacking leaves, has helically arranged bract/scale complexes that arise at right angles from the cone axis in the middle of the cone. The cone axis, ca. 1 mm wide, has a broad cylinder of secondary vascular tissue, and lacks a continuous resin canal system. Bract-scale complexes are laminar, cordate-orbiculate, and upturned distally, consisting primarily of bract tissue with no visible scale tip. The vascular trace to the bract/scale complex originates as a rod that divides laterally into several traces at the level of seed attachment. A single resin canal originates at the base of the bract-scale complex abaxial to the vascular strand, but more distally there are up to ca. 15 large resin canals that form a single row. Two to three inverted winged seeds are attached adaxially near the cone periphery. Cone structure and vascularization are most similar to those in the Cupressaceae, Subfamily Taiwanioideae, differing from living Taiwania cryptomerioides by having up to three seeds/scale rather than two, an abruptly upturned bract tip, in details of bract/scale vasculature, and a cone peduncle lacking leaves. This cone is described as Mukawastrobus satoi Stockey, Nishida and Rothwell. Together with previously described Early to Late Cretaceous taiwanioid seed cones from Mongolia and Hokkaido the new species demonstrates that the taxonomically diagnostic characters of such conifers are as subtle as those of Cretaceous and Cenozoic sequoioid Cupressaceae. This realization emphasizes that evolutionary diversification and turnover among taiwanioid conifers during the Cretaceous and Paleogene are probably far greater than currently recognized.

Grimmiaceae in the Early Cretaceous: Tricarinella crassiphylla gen. et sp. nov. and the value of anatomically preserved bryophytes.

Background and Aims: Widespread and diverse in modern ecosystems, mosses are rare in the fossil record, especially in pre-Cenozoic rocks. Furthermore, most pre-Cenozoic mosses are known from compression fossils, which lack detailed anatomical information. When preserved, anatomy significantly improves resolution in the systematic placement of fossils. Lower Cretaceous (Valanginian) deposits on Vancouver Island (British Columbia, Canada) contain a diverse anatomically preserved flora including numerous bryophytes, many of which have yet to be characterized. Among them is the grimmiaceous moss described here. Methods: One fossil moss gametophyte preserved in a carbonate concretion was studied in serial sections prepared using the cellulose acetate peel technique. Key Results: Tricarinella crassiphylla gen. et sp. nov. is a moss with tristichous phyllotaxis and strongly keeled leaves. The combination of an acrocarpous condition (inferred based on a series of morphological features), a central conducting strand, a homogeneous leaf costa and a lamina with bistratose portions and sinuous cells, and multicellular gemmae, supports placement of Tricarinella in family Grimmiaceae. Tricarinella is similar to Grimmia, a genus that exhibits broad morphological variability. However, tristichous phyllotaxis and especially the lamina, bistratose at the base but not in distal portions of the leaf, set Tricarinella apart as a distinct genus. Conclusions: Tricarinella crassiphylla marks the oldest record for both family Grimmiaceae and sub-class Dicranidae, providing a hard minimum age (136 million years) for these groups. The fact that this fossil could be placed in an extant family, despite a diminutive size, emphasizes the considerable resolving power of anatomically preserved bryophyte fossils, even when recovered from allochthonous assemblages of marine sediments, such as the Apple Bay flora. Discovery of Tricarinella re-emphasizes the importance of paleobotanical studies as the only approach allowing access to a significant segment of biodiversity, the extinct biodiversity, which is unattainable by other means of investigation.

Resolving the overall pattern of marattialean fern phylogeny.

PREMISE OF THE STUDY: Recent clarification of the distribution of Marattiales through time provides the impetus for "total evidence" phylogenetic analyses of a major fern clade with a rich fossil record. These analyses serve as empirical tests for results from systematic analyses of living species and also of the belief that relationships among living species accurately reflect the overall pattern of phylogeny for clades with an extensive fossil record and a large percentage of extinction. METHODS: Species of living and fossil Marattiaceae are analyzed employing a "total evidence approach" via maximum parsimony. Analyses were conducted using TNT implemented through WinClada. KEY RESULTS: Systematic analyses of living species and of living + extinct species provide roughly concordant topologies for living taxa. However, living species of Marattiales are only one component of a much larger clade with two major subclades. One consists of Psaroniaceae and extends through time to at least the Early Cretaceous. The other consists of Marattiaceae and includes all living species. Various analyses support the generic-level clades of living species from earlier analyses, but the arrangement of such clades varies from analysis to analysis. CONCLUSIONS: Marattiales is a monophyletic group that is extremely common in late Paleozoic and early Mesozoic deposits, with a stem group Psaroniaceae and a crown group Marattiaceae. Because Marattiaceae represents only a small component of overall marattialean diversity, living species alone neither account for evolutionary changes within the clade over time, nor accurately reflect the overall pattern of marattialean fern phylogeny.

Origin of Equisetum: Evolution of horsetails (Equisetales) within the major euphyllophyte clade Sphenopsida.

PREMISE OF THE STUDY: Equisetum is the sole living representative of Sphenopsida, a clade with impressive species richness, a long fossil history dating back to the Devonian, and obscure relationships with other living pteridophytes. Based on molecular data, the crown group age of Equisetum is mid-Paleogene, although fossils with possible crown synapomorphies appear in the Triassic. The most widely circulated hypothesis states that the lineage of Equisetum derives from calamitaceans, but no comprehensive phylogenetic studies support the claim. Using a combined approach, we provide a comprehensive phylogenetic analysis of Equisetales, with special emphasis on the origin of genus Equisetum. METHODS: We performed parsimony phylogenetic analyses to address relationships of 43 equisetalean species (15 extant, 28 extinct) using a combination of morphological and molecular characters. KEY RESULTS: We recovered Equisetaceae + Neocalamites as sister to Calamitaceae + a clade of Angaran and Gondwanan horsetails, with the four groups forming a clade that is sister to Archaeocalamitaceae. The estimated age for the Equisetum crown group is mid-Mesozoic. CONCLUSIONS: Modern horsetails are not nested within calamitaceans; instead, both groups have explored independent evolutionary trajectories since the Carboniferous. Diverse fossil taxon sampling helps to shed light on the position and relationships of equisetalean lineages, of which only a tiny remnant is present within the extant flora. Understanding these relationships and early character configurations of ancient plant clades as Equisetales provide useful tests of hypotheses about overall phylogenetic relationships of euphyllophytes and foundations for future tests of molecular dates with paleontological data.

Developmental programmes in the evolution of Equisetum reproductive morphology: a hierarchical modularity hypothesis.

Background: The origin of the Equisetum strobilus has long been debated and the fossil record has played an important role in these discussions. The paradigm underlying these debates has been the perspective of the shoot as node-internode alternation, with sporangiophores attached at nodes. However, fossils historically excluded from these discussions (e.g. Cruciaetheca and Peltotheca ) exhibit reproductive morphologies that suggest attachment of sporangiophores along internodes, challenging traditional views. This has rekindled discussions around the evolution of the Equisetum strobilus, but lack of mechanistic explanations has led discussions to a stalemate. Scope: A shift of focus from the node-internode view to a perspective emphasizing the phytomer as a modular unit of the shoot, frees the debate of homology constraints on the nature of the sporangiophore and inspires a mechanism-based hypothesis for the evolution of the strobilus. The hypothesis, drawing on data from developmental anatomy, regulatory mechanisms and the fossil record, rests on two tenets: (1) the equisetalean shoot grows by combined activity of the apical meristem, laying down the phytomer pattern, and intercalary meristems responsible for internode elongation; and (2) activation of reproductive growth programmes in the intercalary meristem produces sporangiophore whorls along internodes. Conclusions: Hierarchical expression of regulatory modules responsible for (1) transition to reproductive growth; (2) determinacy of apical growth; and (3) node-internode differentiation within phytomers, can explain reproductive morphologies illustrated by Cruciaetheca (module 1 only), Peltotheca (modules 1 and 2) and Equisetum (all three modules). This model has implications - testable by studies of the fossil record, phylogeny and development - for directionality in the evolution of reproductive morphology ( Cruciaetheca - Peltotheca - Equisetum ) and for the homology of the Equisetum stobilus. Furthermore, this model implies that sporangiophore development is independent of node-internode identity, suggesting that the sporangiophore represents the expression of an ancestral euphyllophyte developmental module that pre-dates the evolution of leaves.

Extending the fossil record of Polytrichaceae: Early Cretaceous Meantoinea alophosioides gen. et sp. nov., permineralized gametophytes with gemma cups from Vancouver Island.

PREMISE OF THE STUDY: Diverse in modern ecosystems, mosses are dramatically underrepresented in the fossil record. Furthermore, most pre-Cenozoic mosses are known only from compression fossils, lacking detailed anatomical information. When preserved, anatomy vastly improves resolution in the systematic placement of fossils. Lower Cretaceous deposits at Apple Bay (Vancouver Island, British Columbia, Canada) contain a diverse anatomically preserved flora that includes numerous bryophytes, many of which have yet to be characterized. Among them is a polytrichaceous moss that is described here. METHODS: Fossil moss gametophytes preserved in four carbonate concretions were studied in serial sections prepared using the cellulose acetate peel technique. KEY RESULTS: We describe Meantoinea alophosioides gen. et sp. nov., a polytrichaceous moss with terminal gemma cups containing stalked, lenticular gemmae. Leaves with characteristic costal anatomy, differentiated into sheathing base and free lamina and bearing photosynthetic lamellae, along with a conducting strand in the stem, place Meantoinea in family Polytrichaceae. The bistratose leaf lamina with an adaxial layer of mamillose cells, short photosynthetic lamellae restricted to the costa, and presence of gemma cups indicate affinities with basal members of the Polytrichaceae, such as Lyellia, Bartramiopsis, and Alophosia. CONCLUSIONS: Meantoinea alophosioides enriches the documented moss diversity of an already-diverse Early Cretaceous plant fossil assemblage. This is the third moss described from the Apple Bay plant fossil assemblage and represents the first occurrence of gemma cups in a fossil moss. It is also the oldest unequivocal record of Polytrichaceae, providing a hard minimum age for the group of 136 million years.

Phylogenetic diversification of Early Cretaceous seed plants: The compound seed cone of Doylea tetrahedrasperma.

PREMISE OF THE STUDY: Discovery of cupulate ovules of Doylea tetrahedrasperma within a compact, compound seed cone highlights the rich diversity of fructification morphologies, pollination biologies, postpollination enclosure of seeds, and systematic diversity of Early Cretaceous gymnosperms. METHODS: Specimens were studied using the cellulose acetate peel technique, three-dimensional reconstructions (in AVIZO), and morphological phylogenetic analyses (in TNT). KEY RESULTS: Doylea tetrahedrasperma has bract/fertile short shoot complexes helically arranged within a compact, compound seed cone. Complexes diverge from the axis as a single unit and separate distally into a free bract tip and two sporophylls. Each sporophyll bears a single, abaxial seed, recurved toward the cone axis, that is enveloped after pollinaton by sporophyll tissue, forming a closed cupule. Ovules are pollinated by bisaccate grains captured by micropylar pollination horns. CONCLUSIONS: The unique combination of characters shown by D. tetrahedrasperma includes the presence of cupulate seeds borne in conifer-like compound seed cones, an ovuliferous scale analogue structurally equivalent to the ovulate stalk of Ginkgo biloba, gymnospermous pollination, and nearly complete enclosure of mature seeds. These features characterize the Doyleales ord. nov., clearly distinguish it from the seed fern order Corystospermales, and allow for recognition of another recently described Early Cretaceous seed plant as a second species in genus Doylea. A morphological phylogenetic analysis highlights systematic relationships of the Doyleales ord. nov. and emphasizes the explosive phylogenetic diversification of gymnosperms that was underway at the time when flowering plants may have originated and/or first began to radiate.

Exploring the fossil history of pleurocarpous mosses: Tricostaceae fam. nov. from the Cretaceous of Vancouver Island, Canada.

PREMISE OF THE STUDY: Mosses, very diverse in modern ecosystems, are currently underrepresented in the fossil record. For the pre-Cenozoic, fossil mosses are known almost exclusively from compression fossils, while anatomical preservation, which is much more taxonomically informative, is rare. The Lower Cretaceous of Vancouver Island (British Columbia, Canada) hosts a diverse anatomically preserved flora at Apple Bay. While the vascular plant component of the Apple Bay flora has received much attention, the numerous bryophytes identified at the locality have yet to be characterized. METHODS: Fossil moss gametophytes in more than 20 carbonate concretions collected from the Apple Bay locality on Vancouver Island were studied in serial sections prepared using the cellulose acetate peel technique. KEY RESULTS: We describe Tricosta plicata gen. et sp. nov., a pleurocarpous moss with much-branched gametophytes, tricostate plicate leaves, rhizoid-bearing bases, and delicate gametangia (antheridia and archegonia) borne on specialized branches. A new family of hypnanaean mosses, Tricostaceae fam. nov., is recognized based on the novel combination of characters of T. plicata. CONCLUSIONS: Tricosta plicata reveals pleurocarpous moss diversity unaccounted for in extant floras. This new moss adds the first bryophyte component to an already diverse assemblage of vascular plants described from the Early Cretaceous at Apple Bay and, as the oldest representative of the Hypnanae, provides a hard minimum age for the group (136 Ma).

Middle Jurassic evidence for the origin of Cupressaceae: A paleobotanical context for the roles of regulatory genetics and development in the evolution of conifer seed cones.

PREMISE OF THE STUDY: Triassic and Jurassic fossils record structural changes in conifer seed cones through time, provide the earliest evidence for crown-group conifer clades, and further clarify sister-group relationships of modern conifer families. A new and distinct seed-cone from the Isle of Skye in western Scotland provides the oldest detailed evidence for the ancestral morphology of the phylogenetically contentious family Cupressaceae. METHODS: A single isolated cone was prepared as serial sections by the cellulose acetate peel technique, mounted on microscope slides, and viewed and photographed using transmitted light. The three-dimensional structure of the cone was first reconstructed from the serial sections and then refined through imaging with x-ray microtomography. KEY RESULTS: Scitistrobus duncaanensis, gen. et sp. nov., is a 7.5 mm-diameter cylindrical seed cone with helically arranged bract-scale complexes in which three scale tips separate from a large bract, each tip bearing one adaxial seed. Seeds are near-inverted, show 180° rotational symmetry, and have a diminutive wing in the major plane. CONCLUSIONS: Scitistrobus duncaanensis extends the fossil record for anatomically preserved seed cones of the Cupressaceae backward from the Upper Jurassic to the Aalenian Stage of the Middle Jurassic. The cone displays a previously unknown combination of characters that we regard as diagnostic for seed cones of early-divergent Cupressaceae and helps to clarify the sequence of structural changes that occurred during the transition from ancestral voltzialean conifers to morphologically recognizable Cupressaceae. Hypotheses of homology underpinning such transformational series can be tested by ongoing reciprocal illumination between the morphology of fossil taxa and the morphogenesis and developmental genetics of their extant crown-group relatives.

Hughmillerites vancouverensis sp. nov. and the Cretaceous diversification of Cupressaceae.

UNLABELLED: • PREMISE OF THE STUDY: Two ovulate conifer cones, one of which is attached terminally to a short leafy shoot, reveal the presence of a new species of Hughmillerites in the Early Cretaceous Apple Bay flora of Vancouver Island, British Columbia, Canada. This ancient conifer expands the diversity of Cupressaceae in the Mesozoic and reveals details about the evolution of Subfamily: Cunninghamioideae.• METHODS: Specimens were studied from anatomical sections prepared using the cellulose acetate peel technique.• KEY RESULTS: Vegetative shoots have helically arranged leaves that are Cunninghamia-like. Seed cones have many helically arranged bract/scale complexes in which the bract is larger than the ovuliferous scale. Each ovuliferous scale has three free tips that separate from the bract immediately distal to an inverted seed. Several ovuliferous scales show interseminal ridges between seeds.• CONCLUSIONS: This study documents a new extinct species of cunninghamioid conifers, Hughmillerites vancouverensis, expanding the record of the genus from the Late Jurassic to the Early Cretaceous. This new extinct species emphasizes the important role that conifers from subfamily Cunninghamioideae played in the initial evolutionary radiation of Cupressaceae. In light of recent findings in conifer regulatory genetics, we use H. vancouverensis to hypothesize that variations of expression in certain gene homologues played an important role in the evolution of the cupressaceous ovuliferous scale.

Plant evolution at the interface of paleontology and developmental biology: An organism-centered paradigm.

Paleontology yields essential evidence for inferring not only the pattern of evolution, but also the genetic basis of evolution within an ontogenetic framework. Plant fossils provide evidence for the pattern of plant evolution in the form of transformational series of structure through time. Developmentally diagnostic structural features that serve as "fingerprints" of regulatory genetic pathways also are preserved by plant fossils, and here we provide examples of how those fingerprints can be used to infer the mechanisms by which plant form and development have evolved. When coupled with an understanding of variations and systematic distributions of specific regulatory genetic pathways, this approach provides an avenue for testing evolutionary hypotheses at the organismal level that is analogous to employing bioinformatics to explore genetics at the genomic level. The positions where specific genes, gene families, and developmental regulatory mechanisms first appear in phylogenies are correlated with the positions where fossils with the corresponding structures occur on the tree, thereby yielding testable hypotheses that extend our understanding of the role of developmental changes in the evolution of the body plans of vascular plant sporophytes. As a result, we now have new and powerful methodologies for characterizing major evolutionary changes in morphology, anatomy, and physiology that have resulted from combinations of genetic regulatory changes and that have produced the synapomorphies by which we recognize major clades of plants.

The seed cone Eathiestrobus gen. nov.: fossil evidence for a Jurassic origin of Pinaceae.

PREMISE OF THE STUDY: Pinaceae and nonpinoid species are sister groups within the conifer clade as inferred from molecular systematic comparisons of living species and therefore should have comparable geological ages. However, the fossil record for the nonpinoid lineage of extant conifer families is Triassic, nearly 100 million years older than the oldest widely accepted Lower Cretaceous record for Pinaceae. An anatomically preserved fossil conifer seed cone described here extends the stratigraphic range of Pinaceae nearly 30 million years, thus reducing the apparent discrepancy between evidence from the fossil record and inferences from systematic studies of living species. METHODS: Material was prepared as serial thin sections by the cellulose acetate peel technique, mounted on microscope slides, and viewed and photographed using transmitted light. KEY RESULTS: A large cylindrical cone consisting of bract-scale complexes that diverge from the cone axis in a helical phyllotaxis has bracts and scales that separate from each other in the midregion and are of equal length and of nearly equal width. The cone has two inverted and winged seeds that are attached to the adaxial surface of each cone scale and, thus, represents an early member of the Pinaceae. CONCLUSIONS: Eathiestrobus mackenziei gen. et sp. nov. extends the fossil record for well-documented members of the family Pinaceae from the Lower Cretaceous to the Kimmeridgian Stage of the Upper Jurassic. This species also clarifies the set of characters that are diagnostic for seed cones of Pinaceae and reveals possible plesiomorphic characters for seed cones of the family.

Seed cone anatomy of Cheirolepidiaceae (Coniferales): reinterpreting Pararaucaria patagonica Wieland.

PREMISE OF THE STUDY: Seed cone morphology and anatomy reflect some of the most important changes in the phylogeny and evolutionary biology of conifers. Reexamination of the enigmatic Jurassic seed cone Pararaucaria patagonica reveals previously unknown systematically informative characters that demonstrate affinities with the Cheirolepidiaceae. This paper documents, for the first time, internal anatomy for seed cones of this important extinct Mesozoic conifer family, which may represent the ghost lineage leading to modern Pinaceae. METHODS: Morphology and anatomy of cones from the Jurassic La Matilde Formation in Patagonia are described from a combination of polished wafers and thin section preparations. New photographic techniques are employed to reveal histological details of thin sections in which organic cell wall remains are not preserved. Specific terminology for conifer seed cones is proposed to help clarify hypotheses of homology for the various structures of the cones. KEY RESULTS: Specimens are demonstrated to have trilobed ovuliferous scale tips along with a seed enclosing pocket of ovuliferous scale tissue. Originally thought to represent a seed wing in P. patagonica, this pocket-forming tissue is comparable to the flap of tissue covering seeds of compressed cheirolepidiaceous cones and is probably the most diagnostic character for seed cones of the family. CONCLUSIONS: Pararaucaria patagonica is assigned to Cheirolepidiaceae, documenting anatomical features for seed cones of the family and providing evidence for the antiquity of pinoid conifers leading to the origin of Pinaceae. A list of key morphological and anatomical characters for seed cones of Cheirolepidiaceae is developed to facilitate assignment of a much broader range of fossil remains to the family. This confirms the presence of Cheirolepidiaceae in the Jurassic of the Southern Hemisphere, which was previously suspected from palynological records.

Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm.

Fossils constitute the principal repository of data that allow for independent tests of hypotheses of biological evolution derived from observations of the extant biota. Traditionally, transformational series of structure, consisting of sequences of fossils of the same lineage through time, have been employed to reconstruct and interpret morphological evolution. More recently, a move toward an updated paradigm was fueled by the deliberate integration of developmental thinking in the inclusion of fossils in reconstruction of morphological evolution. The vehicle for this is provided by structural fingerprints-recognizable morphological and anatomical structures generated by (and reflective of) the deployment of specific genes and regulatory pathways during development. Furthermore, because the regulation of plant development is both modular and hierarchical in nature, combining structural fingerprints recognized in the fossil record with our understanding of the developmental regulation of those structures produces a powerful tool for understanding plant evolution. This is particularly true when the systematic distribution of specific developmental regulatory mechanisms and modules is viewed within an evolutionary (paleo-evo-devo) framework. Here, we discuss several advances in understanding the processes and patterns of evolution, achieved by tracking structural fingerprints with their underlying regulatory modules across lineages, living and fossil: the role of polar auxin regulation in the cellular patterning of secondary xylem and the parallel evolution of arborescence in lycophytes and seed plants; the morphology and life history of early polysporangiophytes and tracheophytes; the role of modularity in the parallel evolution of leaves in euphyllophytes; leaf meristematic activity and the parallel evolution of venation patterns among euphyllophytes; mosaic deployment of regulatory modules and the diverse modes of secondary growth of euphyllophytes; modularity and hierarchy in developmental regulation and the evolution of equisetalean reproductive morphology. More generally, inclusion of plant fossils in the evo-devo paradigm has informed discussions on the evolution of growth patterns and growth responses, sporophyte body plans and their homology, sequences of character evolution, and the evolution of reproductive systems.