Fossil palm reading: using fruits to reveal the deep roots of palm diversity.

PREMISE: Fossils are essential for understanding evolutionary history because they provide direct evidence of past diversity and geographic distributions. However, resolving systematic relationships between fossils and extant taxa, an essential step for many macroevolutionary studies, requires extensive comparative work on morphology and anatomy. While palms (Arecaceae) have an excellent fossil record that includes numerous fossil fruits, many are difficult to identify due in part to limited comparative data on modern fruit structure. METHODS: We studied fruits of 207 palm species, representing nearly every modern genus, using X-ray microcomputed tomography. We then developed a morphological data set to test whether the fossil record of fruits can improve our understanding of palm diversity in the deep past. To evaluate the accuracy with which this data set recovers systematic relationships, we performed phylogenetic pseudofossilization analyses. We then used the data set to investigate the phylogenetic relationships of five previously published fossil palm fruits. RESULTS: Phylogenetic analyses of fossils and pseudofossilization of extant taxa show that fossils can be placed accurately to the tribe and subtribe level with this data set, but node support must be considered. The phylogenetic relationships of the fossils suggest origins of many modern lineages in the Cretaceous and early Paleogene. Three of these fossils are suitable as new node calibrations for palms. CONCLUSIONS: This work improves our knowledge of fruit structure in palms, lays a foundation for applying fossil fruits to macroevolutionary studies, and provides new insights into the evolutionary history and early diversification of Arecaceae.

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

[This corrects the article DOI: 10.7717/peerj.4580.].

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 (Viracarponhexaspermum and Viracarponelongatum), 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.

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.

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.

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.

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.