Extending the fossil record of the Polytrichaceae (Bryophyta): insights from the early Cretaceous of Vancouver Island, Canada

Diverse in modern ecosystems, mosses are dramatically underrepresented in the fossil record. Furthermore, most pre-Cenozoic mosses are known only from compression fossils, which lack detailed anatomical information. 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 as Meantoinea alophosioides gen. et sp. nov. Meantoinea alophosioides represents the first occurrence of gemma cups in a fossil moss and is the oldest unequivocal record of Polytrichaceae, providing a hard minimum age for the group of 136 Ma (Valanginian). In order to assess the phylogenetic relationships of fossil Polytrichaceae (including Meantoinea) and compare hypotheses of relationships recovered using molecular vs morphological methods, I conducted a comprehensive morphology-based phylogenetic study of the family. This phylogenetic study used a dataset of 100 morphological characters scored for 44 species of acrocarpous mosses, and parsimony as the optimality criterion. Results of the phylogenetic analysis suggest that morphology is useful in resolving phylogenetic relationships in the Polytrichaceae and that both fossil Polytrichaceae have stable phylogenetic relationships. However, rooting experiments demonstrate that there is no superior way to root analyses and indicate that relationships within the family are best evaluated using unrooted networks without outgroup taxa. These rooting problems suggest that additional information is needed to understand the phylogenetic relationships of Polytrichaceae. Such additional information could come from fossils of stem group polytrichaceous mosses, which await discovery

Permineralized Mesozoic Moss Gametophytes and their Implications for Bryophyte Evolution

Mosses (Phylum Bryophyta) are widely considered to be among the most ancient groups of land plants (embryophytes) and they are the second most speciose embryophyte phylum with ~13,000 extant species. Despite their diversity and antiquity, mosses have a limited fossil record, which primarily consists of gametophytes entombed in Cenozoic amber. However, surveys of Mesozoic floras from North and South America have recently uncovered a wealth of permineralized moss gametophytes. These fossils present the first opportunity to explore macroevolutionary trends in mosses over deep geologic time, with rich sampling of pre-Cenozoic diversity. The over-arching goal of this dissertation is to explore moss evolution over geologic time, using these recently discovered permineralized gametophytes. There are four main objectives: 1) document moss diversity in Late Jurassic and Cretaceous deposits by characterizing anatomically preserved fossil mosses, 2) investigate patterns in moss biogeography using data from the fossil record, 3) understand the longevity of moss genera over geologic time, and 4) explore the hypothesis that modern moss lineages diversified as part of the Cretaceous Terrestrial Revolution using paleontological data. Herein, six new taxa are characterized based on permineralized gametophytes from one Late Jurassic and three Cretaceous deposits. All fossils were studied using light microscopy. In Chapter 2, a permineralized acrocarpous moss gametophyte from the Late Jurassic of Patagonia, Argentina, is described. This fossil was prepared using the petrographic thin sectioning technique. The gametophyte shoot is unbranched, and leaves have a broad sheathing leaf base that narrows distally, forming a free leaf blade. Costa is strong, with an adaxial epidermis of bulging-mammillose cells, subtended by guide cells and a single abaxial stereid band. An abaxial epidermis is lacking. In the free leaf blade, the lamina is bistratose, with an adaxial layer of bulging-mammillose cells. This fossil gametophyte displays a novel combination of characters that suggest basal affinities within the families Timmiellaceae or Polytrichaceae. Both of these families are members of a grade within Subphylum Bryophytina basal to Subclass Bryidae. Therefore, this fossil is described as a new genus and species assignable to Subphylum Bryophytina, Heinrichsiella patagonica gen. et sp. nov. Heinrichsiella is the oldest evidence of this basal grade within Subphylum Bryophytina by at least 15 Ma. In Chapter 3, a permineralized moss gametophyte assignable to the extant genus Cynodontium is described from the Late Cretaceous of the North Slope of Alaska. This fossil was permineralized in a terrestrial limestone and prepared using the cellulose acetate peel technique. The moss gametophyte branches irregularly and has leaves with a broad base, narrow blade, and excurrent costa. Leaf margins are narrowly recurved basally, becoming bistratose and denticulate distally. Costa is strong and composed of a poorly defined epidermis, guide cells, and thin-walled substereids. Leaf blade is keeled basally, becoming channeled distally. Laminar cells are subquadrate or rectangular proximally, becoming quadrate distally. This fossil has a combination of gametophytic characters diagnostic of the extant genus Cynodontium, but displays a novel combination of characters that are distinct from any extant species of that genus. Therefore, this fossil is described as Cynodontium luthii sp. nov. This species is the oldest evidence for Cynodontium by at least 15 Ma and reveals that some genera found in the High Arctic today also lived in the region during the Late Cretaceous, when it experienced a temperate climate. In Chapter 4, three new species of the extant genus Sphagnum are described based on permineralized gametophytes from the Late Santonian to Campanian of Vancouver Island, Canada. These fossils were permineralized in near-shore marine calcareous concretions and prepared using the cellulose acetate peel technique. All three species have unistratose leaves that are composed of smaller cells (chlorocysts) that alternate with larger, porose cells (hyalocysts). Collectively, these features are diagnostic of Sphagnum. The three species are most easily distinguished based on their stem anatomy. Stems of Sphagnum species one have a unistratose hyalodermis, while stems of Sphagnum species two have a multistratose hyalodermis, and stems of Sphagnum species three completely lack a hyalodermis. Taxonomic comparisons with extant species of Sphagnum are difficult due to the fragmentary nature of the specimens. Sphagnum species one and two have combinations of features found in several extant sections of Sphagnum. However, the absence of a hyalodermis is a character that is only found in some species of Sphagnum Section Cuspidata. Therefore, Sphagnum species three can be assigned to Section Cuspidata and is the only pre-Pleistocene evidence for that section. These fossils also represent the first reports of permineralized Sphagnum gametophytes and reveal that Sphagnum was anatomically diverse by the Late Cretaceous, which is far earlier than predicted by some molecular dating analyses. In Chapter 5, permineralized moss gametophytes assignable to the family Leucobryaceae are described from the Valanginian (~136 Ma) of Vancouver Island, Canada. These fossils were permineralized in near-shore marine calcareous concretions and prepared using the cellulose acetate peel technique. The gametophyte shoots are irregularly branched, leaves are almost entirely comprised of an expanded costa. Lamina is restricted to the sheathing leaf base and composed of small-diameter porose cells that are isodiametric in cross section. Anatomically, the costa is comprised of larger porose cells that are rectangular in cross section (leucocysts) and much smaller, thicker-walled cells, which are triangular in cross section for most of the leaf (chlorocysts). Costa is typically homostrosic, with a single layer of leucocysts on either side of centric chlorocysts. The unusual leaf anatomy of these fossils is diagnostic of the leucobryoid clade within the family Leucobryaceae. However, the fossils display a mosaic of characters, combining features of two leucobryoid genera (Leucobryum and Steyermarkiella). Therefore, they will be assigned to a new genus and species. These fossils are the oldest evidence of the family Leucobryaceae by at least 88 Ma and the oldest evidence of the leucobryoid clade within this family by >115 Ma. In Chapter 6, the role of paleontological data in bryophyte systematics is summarized based on a comprehensive review of the paleobryological literature, considering techniques for integrating fossils into evolutionary analyses with extant plants as well as aspects of bryophyte structure and ecology relevant to taphonomy. Bryophytes are unusual in that the group has a deep evolutionary history, but a sparse fossil record. The paucity of bryophyte fossils is driven by phenotypic and ecological features related to the small size and patchy ecological distributions of most members of the group as well as incomplete exploration of the fossil record. However, fossils provide unique insight on the evolution of organisms (including bryophytes), over deep time. They are the only means to independently test hypotheses about evolution generated from extant bryophytes and are essential for making accurate inferences regarding speciation and extinction rates, patterns of morphological evolution, and biogeography. The review concludes that development of robust morphological datasets for bryophytes, that would allow fossils to be integrated into macroevolutionary analyses alongside extant plants as well as focused efforts to uncover and describe pre-Cenozoic bryofloras are essential for bringing deep-time evolutionary perspectives to bryophyte systematics

The role of paleontological data in bryophyte systematics

Systematics reconstructs tempo and mode in biological evolution by resolving the phylogenetic fabric of biodiversity. The staggering duration and complexity of evolution, coupled with loss of information (extinction), render exhaustive reconstruction of the evolutionary history of life unattainable. Instead, we sample its products-phenotypes and genotypes-to generate phylogenetic hypotheses, which we sequentially reassess and update against new data. Current consensus in evolutionary biology emphasizes fossil integration in total-evidence analyses, requiring in-depth understanding of fossils-age, phenotypes, and systematic affinities-and a detailed morphological framework uniting fossil and extant taxa. Bryophytes present a special case: deep evolutionary history but sparse fossil record and phenotypic diversity encompassing small dimensional scales. We review how these peculiarities shape fossil inclusion in bryophyte systematics. Paucity of the bryophyte fossil record, driven primarily by phenotypic (small plant size) and ecological constraints (patchy substrate-hugging populations), and incomplete exploration, results in many morphologically isolated, taxonomically ambiguous fossil taxa. Nevertheless, instances of exquisite preservation and pioneering studies demonstrate the feasibility of including bryophyte fossils in evolutionary inference. Further progress will arise from developing extensive morphological matrices for bryophytes, continued exploration of the fossil record, re-evaluation of previously described fossils, and training specialists in identification and characterization of bryophyte fossils, and in bryophyte morphology. Unlocking the severely underutilized potential of the bryophyte fossil record for illuminating phylogeny, systematics, and evolution will require, aside from continued exploration, development of extensive morphological matrices and trained specialists.Peer reviewe

Palynology of a short sequence of the Lower Devonian Beartooth Butte Formation at Cottonwood Canyon (Wyoming): age, depositional environments and plant diversity

The Beartooth Butte Formation hosts the most extensive Early Devonian macroflora of western North America. The age of the flora at Cottonwood Canyon (Wyoming) has been constrained to the Lochkovian–Pragian interval, based on fish biostratigraphy and unpublished palynological data. We present a detailed palynological analysis of the plant-bearing layers at Cottonwood Canyon. The palynomorphs consist of 32 spore, five cryptospore, two prasinophycean algae and an acritarch species. The stratigraphic ranges of these palynomorphs indicate a late Lochkovian or Pragian age, confirming previous age assignments. Analysis of samples from three different depositional environments of the plant-bearing sequence (layers with in situ lycophyte populations, flood layers that buried those populations and an organic matter accumulation zone within a flood layer) demonstrate distinct palynofacies. Comparisons between palynomorph and plant macrofossil diversity reveal some discrepancies. Whereas zosterophylls and lycophytes, most diverse and abundant among the macrofossils, have only one known corresponding spore type (assignable to zosterophylls) in the palynomorph assemblage, the trimerophytes, rare in the macrofossil assemblage, are represented by three spore types. Some of these discrepancies reflect taphonomic differences between the macrofossils and palynomorphs, while others could be due to the fact that the parent plants of most palynomorph types in the Cottonwood Canyon assemblage are unknown. These observations emphasize the need for concerted efforts to bring together the knowledge of macro- and microfloras within Early Devonian localities. Nevertheless, given the palaeophytogeographic significance of the Beartooth Butte Formation flora, its palynofossil and macrofossil assemblages, taken together, provide new data relevant to future discussions of Early Devonian biogeography.Fil: Noetinger, Maria Sol. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales "Bernardino Rivadavia"; ArgentinaFil: Bippus, Alexander C.. State University of Oregon; Estados UnidosFil: Tomescu, Alexander M. F.. Humboldt State University; Estados Unido

Wanted dead or alive (probably dead): Stem group Polytrichaceae

Premise of the Study: The Polytrichaceae are a widespread and morphologically isolated moss lineage. Early attempts to characterize phylogenetic relationships within the family suggested that morphology is not phylogenetically informative. Two well-characterized fossils similar to basal and derived Polytrichaceae (Meantoinea alophosioides and Eopolytrichum antiquum, respectively), are known from Cretaceous rocks. To assess the phylogenetic positions of these fossils and compare hypotheses of relationships recovered using molecular vs. morphological methods, we conducted a comprehensive morphology-based phylogenetic study of Polytrichaceae. Methods: We evaluated the phylogenetic relationships of Polytrichaceae using a data set of 100 morphological characters (including 11 continuously varying traits codified as continuous characters) scored for 44 species of acrocarpous mosses and parsimony as the optimality criterion. Key Results: Continuous characters significantly increased the resolving power of the analyses. The overall ingroup topology was sensitive to rooting as determined by outgroup selection, with some analyses yielding results that were incongruent with those of molecular studies. Both fossils had stable phylogenetic relationships, irrespective of outgroup sampling. Conclusions: Our results suggest that morphology is useful in resolving phylogenetic relationships in the Polytrichaceae, if both discrete and continuous characters are used. However, our rooting experiments demonstrate that there is no superior way to root analyses and indicate that relationships within the family are best evaluated using unrooted networks without outgroup taxa. These rooting problems suggest that additional information is needed to understand the phylogenetic relationships of Polytrichaceae. Such additional information could come from fossils of stem group polytrichaceous mosses, which await discovery.Fil: Bippus, Alexander C.. Humboldt State University; Estados UnidosFil: Escapa, Ignacio Hernán. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Museo Paleontológico Egidio Feruglio; ArgentinaFil: Tomescu, Alexandru M. F.. Humboldt State University; Estados Unido

Fossil fern rhizomes as a model system for exploring epiphyte community structure across geologic time: evidence from Patagonia

In extant ecosystems, complex networks of ecological interactions between organisms can be readily studied. In contrast, understanding of such interactions in ecosystems of the geologic past is incomplete. Specifically, in past terrestrial ecosystems we know comparatively little about plant biotic interactions besides saprotrophy, herbivory, mycorrhizal associations, and oviposition. Due to taphonomic biases, epiphyte communities are particularly rare in the plant-fossil record, despite their prominence in modern ecosystems. Accordingly, little is known about how terrestrial epiphyte communities have changed across geologic time. Here, we describe a tiny in situ fossil epiphyte community that sheds light on plant-animal and plant-plant interactions more than 50 million years ago.MethodsA single silicified Todea (Osmundaceae) rhizome from a new locality of the early Eocene (ca. 52 Ma) Tufolitas Laguna del Hunco (Patagonia, Argentina) was studied in serial thin sections using light microscopy. The community of organisms colonizing the tissues of the rhizome was characterized by identifying the organisms and mapping and quantifying their distribution. A 200 × 200 µm grid was superimposed onto the rhizome cross section, and the colonizers present at each node of the grid were tallied.ResultsPreserved in situ, this community offers a rare window onto aspects of ancient ecosystems usually lost to time and taphonomic processes. The community is surprisingly diverse and includes the first fossilized leafy liverworts in South America, also marking the only fossil record of leafy bryophyte epiphytes outside of amber deposits; as well as several types of fungal hyphae and spores; microsclerotia with possible affinities in several ascomycete families; and evidence for oribatid mites.DiscussionThe community associated with the Patagonian rhizome enriches our understanding of terrestrial epiphyte communities in the distant past and adds to a growing body of literature on osmundaceous rhizomes as important hosts for component communities in ancient ecosystems, just as they are today. Because osmundaceous rhizomes represent an ecological niche that has remained virtually unchanged over time and space and are abundant in the fossil record, they provide a paleoecological model system that could be used to explore epiphyte community structure through time.Fil: Bippus, Alexander C.. University of Oregon; Estados UnidosFil: Escapa, Ignacio Hernán. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Museo Paleontológico Egidio Feruglio; ArgentinaFil: Wilf, Peter. State University of Pennsylvania; Estados UnidosFil: Tomescu, Alexandru M. F.. Humboldt State University; Estados Unido

Heinrichsiella patagonica gen. Et sp. nov.: A permineralized acrocarpous moss from the jurassic of patagonia

Premise of research. Today, mosses are the second most speciose lineage of land plants and are important components of many ecosystems. However, in spite of their diversity and ecological importance in the modern biota, mosses are rare in the fossil record, especially prior to the Cenozoic. Therefore, every new report of a pre-Cenozoic moss deeply enriches our understanding of their evolution. Pre-Cenozoic permineralized mosses represent particularly exciting discoveries because a thorough understanding of the organism is possible. Here, we present the first permineralized Jurassic moss. Methodology. A single chert block from the Cañadón Nahuel locality of the Jurassic (178–151 Ma) Deseado Massif in Santa Cruz Province, Patagonia, was polished, and the plants within were examined, revealing a moss gametophyte shoot. A thin section of this chert block was cut and subsequently examined using light microscopy. Pivotal results. We describe Heinrichsiella patagonica gen. et sp. nov., an acrocarpous moss with a novel combination of gametophyte features that suggests basal affinities within either the family Polytrichaceae or the family Timmiellaceae. Both of these families are members of a grade within subphylum Bryophytina basal to subclass Bryidae. Heinrichsiella is the oldest member of this grade by at least 15 million years. Conclusions. Heinrichsiella patagonica is the first report of a moss from the Jurassic Deseado Massif hydrothermal cherts of Patagonia. This fossil reveals that stem group members of extant acrocarpous moss families lived during the Jurassic, implicating the Jurassic as a critical time for understanding the evolution of higher-level moss taxa.Fil: Bippus, Alexander C.. State University of Oregon; Estados UnidosFil: Savoretti, María Adolfina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Escapa, Ignacio Hernán. Museo Paleontologico Egidio Feruglio; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: García Massini, Juan Leandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja. - Universidad Nacional de La Rioja. Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja. - Universidad Nacional de Catamarca. Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja. - Secretaría de Industria y Minería. Servicio Geológico Minero Argentino. Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja. - Provincia de La Rioja. Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja; ArgentinaFil: Guido, Diego Martin. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. Instituto de Recursos Minerales. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Instituto de Recursos Minerales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentin

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.Fil: Savoretti, María Adolfina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Botánica Darwinion. Academia Nacional de Ciencias Exactas, Físicas y Naturales. Instituto de Botánica Darwinion; ArgentinaFil: Bippus, Alexander C.. Humboldt State University; Estados UnidosFil: Stockey, Ruth A.. State University of Oregon; Estados UnidosFil: Rothwell, Gar W.. State University of Oregon; Estados UnidosFil: Tomescu, Alexandru M. F.. State University of Oregon; Estados Unido

Dating the evolution of the complex thalloid liverworts (Marchantiopsida): total-evidence dating analysis supports a Late Silurian-Early Devonian origin and post-Mesozoic morphological stasis

Divergence times based on molecular clock analyses often differ from those derived from total-evidence dating (TED) approaches. For bryophytes, fossils have been excluded from previous assessments of divergence times, and thus, their utility in dating analyses remains unexplored. Here, we conduct the first TED analyses of the complex thalloid liverworts (Marchantiopsida) that include fossils and evaluate macroevolutionary trends in morphological ‘diversity’ (disparity) and rates. Phylogenetic analyses were performed on a combined dataset of 130 discrete characters and 11 molecular markers (sampled from nuclear, plastid and mitochondrial genomes). Taxon sampling spanned 56 extant species – representing all the orders within Marchantiophyta and extant genera within Marchantiales – and eight fossil taxa. Total-evidence dating analyses support the radiation of Marchantiopsida during Late Silurian-Early Devonian (or Middle Ordovician when the outgroup is excluded) and that of Ricciaceae in the Middle Jurassic. Morphological change rate was high early in the history of the group, but it barely increased after Late Cretaceous. Disparity-through-time analyses support a fast increase in diversity until the Middle Triassic (c. 250 Ma), after which phenotypic evolution slows down considerably. Incorporating fossils in analyses challenges previous assumptions on the affinities of extinct taxa and indicates that complex thalloid liverworts radiated c. 125 Ma earlier than previously inferred.Fil: Flores, Jorge Rafael. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Bippus, Alexander C.. No especifíca;Fil: Fernandez de Ullivarri, Carmen. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Suarez, Guillermo Martin. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Hyvönen, Jaakko. University of Helsinki; FinlandiaFil: Tomescu, Alexandru M. F.. California State Polytechnic University Humboldt; Estados Unido