Kelly K. S. Matsunaga

Root evolution at the base of the lycophyte clade: insights from an Early Devonian lycophyte

BACKGROUND AND AIMS The evolution of complex rooting systems during the Devonian had significant impacts on global terrestrial ecosystems and the evolution of plant body plans. However, detailed understanding of the pathways of root evolution and the architecture of early rooting systems is currently lacking. We describe the architecture and resolve the structural homology of the rooting system of an Early Devonian basal lycophyte. Insights gained from these fossils are used to address lycophyte root evolution and homology. METHODS Plant fossils are preserved as carbonaceous compressions at Cottonwood Canyon (Wyoming), in the Lochkovian-Pragian (∼411 Ma; Early Devonian) Beartooth Butte Formation. We analysed 177 rock specimens and documented morphology, cuticular anatomy and structural relationships, as well as stratigraphic position and taphonomic conditions. KEY RESULTS The rooting system of the Cottonwood Canyon lycophyte is composed of modified stems that bear fine, dichotomously branching lateral roots. These modified stems, referred to as root-bearing axes, are produced at branching points of the above-ground shoot system. Root-bearing axes preserved in growth position exhibit evidence of positive gravitropism, whereas the lateral roots extend horizontally. Consistent recurrence of these features in successive populations of the plant preserved in situ demonstrates that they represent constitutive structural traits and not opportunistic responses of a flexible developmental programme. CONCLUSIONS This is the oldest direct evidence for a rooting system preserved in growth position. These rooting systems, which can be traced to a parent plant, include some of the earliest roots known to date and demonstrate that substantial plant-substrate interactions were under way by Early Devonian time. The morphological relationships between stems, root-bearing axes and roots corroborate evidence that positive gravitropism and root identity were evolutionarily uncoupled in lycophytes, and challenge the hypothesis that roots evolved from branches of the above-ground axial system, suggesting instead that lycophyte roots arose as a novel organ.

Temperature and salinity of the Late Cretaceous Western Interior Seaway

The Western Interior Seaway (WIS) was a shallow and expansive body of water that covered the central United States during the Late Cretaceous. Attempts to reconstruct temperatures in the seaway using the oxygen isotopic composition of biogenic carbonates have suffered from uncertainty in the oxygen isotopic composition of seawater (δ 18 O w ) in the semi-restricted basin. We present new reconstructed temperature and δ 18 O w data from marine and estuarine environments in the WIS and freshwater environments in WIS source rivers, derived from clumped isotope analyses of bivalve and gastropod shells. We find temperatures of 5–21 °C, δ 18 O w values below contemporaneous Gulf of Mexico marine sites, and a strong correlation between δ 18 O w and environmental setting. We propose that decreasing δ 18 O w values reflect decreasing salinity driven by an increasing contribution of continental runoff. Using a two-end-member salinity-δ 18 O w mixing model, we estimate salinities of 29–35 psu (practical salinity units) for the deep marine, 20–32 psu for the shallow marine, and 11–26 psu for the estuarine environments of the WIS. New climate model simulations agree with reconstructed temperatures and salinities and suggest the presence of salinity driven stratification within the seaway.

Honeggeriella complexa gen. et sp. nov., a heteromerous lichen from the Lower Cretaceous of Vancouver Island (British Columbia, Canada)

PREMISE OF THE STUDY Colonists of even the most inhospitable environments, lichens are present in all terrestrial ecosystems. Because of their ecological versatility and ubiquity, they have been considered excellent candidates for early colonizers of terrestrial environments. Despite such predictions, good preservation potential, and the extant diversity of lichenized fungi, the fossil record of lichen associations is sparse. Unequivocal lichen fossils are rare due, in part, to difficulties in ascertaining the presence of both symbionts and in characterizing their interactions. This study describes an exceptionally well-preserved heteromerous lichen from the Lower Cretaceous of Vancouver Island. METHODS The fossil occurs in a marine carbonate concretion collected from the Apple Bay locality on Vancouver Island, British Columbia, and was prepared for light microscopy and SEM using the cellulose acetate peel technique. KEY RESULTS The lichen, Honeggeriella complexa gen. et sp. nov., is formed by an ascomycete mycobiont and a chlorophyte photobiont, and exhibits heteromerous thallus organization. This is paired with a mycobiont-photobiont interface characterized by intracellular haustoria, previously not documented in the fossil record. CONCLUSIONS Honeggeriella adds a lichen component to one of the richest and best characterized Early Cretaceous floras and provides a significant addition to the sparse fossil record of lichens. As a heteromerous chlorolichen, it bridges the >350 million-year gap between previously documented Early Devonian and Eocene occurrences.

An organismal concept for Sengelia radicans gen. et sp. nov. – morphology and natural history of an Early Devonian lycophyte

Background and Aims Fossil plants are found as fragmentary remains and understanding them as natural species requires assembly of whole-organism concepts that integrate different plant parts. Such concepts are essential for incorporating fossils in hypotheses of plant evolution and phylogeny. Plants of the Early Devonian are crucial to reconstructing the initial radiation of tracheophytes, yet few are understood as whole organisms. Methods This study assembles a whole-plant concept for the Early Devonian lycophyte Sengelia radicans gen. et sp. nov., based on morphometric data and taphonomic observations from >1000 specimens collected in the Beartooth Butte Formation (Wyoming, USA). Key Results Sengelia radicans occupies a key position between stem-group and derived lycophyte lineages. Sengelia had a rooting system of downward-growing root-bearing stems, formed dense monotypic mats of prostrate shoots in areas that experienced periodic flooding, and was characterized by a life-history strategy adapted for survival after floods, dominated by clonality, and featuring infrequent sexual reproduction. Conclusions Sengelia radicans is the oldest among the very few early tracheophytes for which a detailed, rigorous whole-plant concept integrates morphology, growth habit, life history and growth environment. This plant adds to the diversity of body plans documented among lycophytes and may help elucidate patterns of morphological evolution in the clade.

Microbes and the Fossil Record: Selected Topics in Paleomicrobiology

The study of microbial fossils involves a broad array of disciplines and covers a vast diversity of topics, of which we review a select few, summarizing the state of the art. Microbes are found as body fossils preserved in different modes and have also produced recognizable structures in the rock record (microbialites, microborings). Study of the microbial fossil record and controversies arising from it have provided the impetus for the assembly and refining of powerful sets of criteria for recognition of bona fide microbial fossils. Different types of fossil evidence concur in demonstrating that microbial life was present in the Archean, close to 3.5 billion years ago. Early eukaryotes also fall within the microbial realm and criteria developed for their recognition date the oldest unequivocal evidence close to 2.0 billion years ago (Paleoproterozoic), but Archean microfossils >3 billion years old are strong contenders for earliest eukaryotes. In another dimension of their contribution to the fossil record, microbes play ubiquitous roles in fossil preservation, from facilitating authigenic mineralization to replicating soft tissue with extracellular polymeric substances, forming biofilms that inhibit decay of biological material, or stabilizing sediment interfaces. Finally, studies of the microbial fossil record are relevant to profound, perennial questions that have puzzled humanity and science—they provide the only direct window onto the beginnings and early evolution of life; and the methods and criteria developed for recognizing ancient, inconspicuous traces of life have yielded an approach directly applicable to the search for traces of life on other worlds.

Vascularization of the Selaginella rhizophore: anatomical fingerprints of polar auxin transport with implications for the deep fossil record

The Selaginella rhizophore is a unique and enigmatic organ whose homology with roots, shoots, or neither of the two remains unresolved. Nevertheless, rhizophore-like organs have been documented in several fossil lycophytes. Here we test the homology of these organs through comparisons with the architecture of rhizophore vascularization in Selaginella. We document rhizophore vascularization in nine Selaginella species using cleared whole-mounts and histological sectioning combined with three-dimensional reconstruction. Three patterns of rhizophore vascularization are present in Selaginella and each is comparable to those observed in rhizophore-like organs of fossil lycophytes. More compellingly, we found that all Selaginella species sampled exhibit tracheids that arc backward from the stem and side branch into the rhizophore base. This tracheid curvature is consistent with acropetal auxin transport previously documented in the rhizophore and is indicative of the redirection of basipetal auxin from the shoot into the rhizophore during development. The tracheid curvature observed in Selaginella rhizophores provides an anatomical fingerprint for the patterns of auxin flow that underpin rhizophore development. Similar tracheid geometry may be present and should be searched for in fossils to address rhizophore homology and the conservation of auxin-related developmental mechanisms from early stages of lycophyte evolution.

Reinvestigating an enigmatic Late Cretaceous monocot: morphology, taxonomy, and biogeography of Viracarpon

Angiosperm-dominated floras of the Late Cretaceous are essential for understanding the evolutionary, ecological, and geographic radiation of flowering plants. The Late Cretaceous–early Paleogene Deccan Intertrappean Beds of India contain angiosperm-dominated plant fossil assemblages known from multiple localities in central India. Numerous monocots have been documented from these assemblages, providing a window into an important but poorly understood time in their diversification. One component of the Deccan monocot diversity is the genus Viracarpon, known from anatomically preserved infructescences. Viracarpon was first collected over a century ago and has been the subject of numerous studies. However, resolution of its three-dimensional (3D) morphology and anatomy, as well as its taxonomic affinities, has remained elusive. In this study we investigated the morphology and taxonomy of genus Viracarpon, combining traditional paleobotanical techniques and X-ray micro-computed tomography (μCT). Re-examination of type and figured specimens, 3D reconstructions of fruits, and characterization of structures in multiple planes of section using μCT data allowed us to resolve conflicting interpretations of fruit morphology and identify additional characters useful in refining potential taxonomic affinities. Among the four Viracarpon species previously recognized, we consider two to be valid (Viracarpon hexaspermum and Viracarpon elongatum), and the other two to be synonyms of these. Furthermore, we found that permineralized infructescences of Coahuilocarpon phytolaccoides from the late Campanian of Mexico correspond closely in morphology to V. hexaspermum. We argue that Viracarpon and Coahuilocarpon are congeneric and provide the new combination, Viracarpon phytolaccoides (Cevallos-Ferriz, Estrada-Ruiz & Perez-Hernandez) Matsunaga, S.Y. Smith, & Manchester comb. nov. The significant geographic disjunction between these two occurrences indicates that the genus Viracarpon was widespread and may be present in other Late Cretaceous assemblages. Viracarpon exhibits character combinations not present in any extant taxa and its affinities remain unresolved, possibly representing an extinct member of Alismatales. The character mosaic observed in Viracarpon and the broad distribution of the genus provide new data relevant to understanding early monocot evolution and suggest that the (thus far) largely invisible Late Cretaceous monocot diversification was characterized by enigmatic and/or stem taxa.

Reciprocal Illumination and Fossils Provide Important Perspectives in Plant Evo-devo: Examples from Auxin in Seed-Free Plants

The plant hormone auxin plays an integral role in numerous aspects of plant development, from embryogeny through secondary growth, which has raised the question of whether changes in auxin signaling underlie major morphological changes in land plant evolution. However, the majority of available data on auxin action come from studies of angiosperms, and it is unclear to what extent these data can be applied to other plant lineages, particularly seed-free plants. Here we review the current state of knowledge on auxin and its role in seed-free plant development, with a focus on polar auxin transport, and illustrate the value of using reciprocal illumination approaches that integrate the fossil record for understanding the evolution of plant form and development. Our survey reveals that while there are some differences, particularly between lycophytes and euphyllophytes, the general patterns of polar auxin transport and auxin action appear to be shared among all tracheophytes. Based on these data, we provide insights and testable hypotheses on leaf and rooting system evolution among lycophytes, demonstrating the utility of anatomical fingerprints of development. However, we also find that numerous gaps in our understanding of the roles of auxin in seed-free plants remain that stymie further progress. Filling these gaps will require continuing incremental research on seed-free plant development, from anatomy to developmental genetics, but has broad potential for making significant contributions to our understanding of patterns and processes in plant evolution.