From Plant Press, Vol. 21, No. 3, July 2018.
By Kayleigh Walters and Gary A. Krupnick
This year's Smithsonian Botanical Symposium explored the deep time of botany with the theme, “Plants in the Past: Fossils and the Future.” Seven speakers presented a whirlwind of information over the course of a day, focusing heavily on the benefit brought by developing technologies to the field of paleobotany. The symposium, held on 18 May 2018, convened at the Warner Bros Theater at the National Museum of American History, a change in scenery from past symposia as Natural History’s Baird Auditorium undergoes renovations.
Before the symposium began, the Joseph F. Cullman 3rd Library of Natural History opened its doors to attendees for special tours of the library's paleobotany books. The Library put on display a wide selection of publications that highlight fossil plants, from Boccone's Recherches (1674), through the editions of Scheuchzer's Herbarium diluvianum (1709, 1723), to Brongniart's works in the 19th century, and more. Attendees learned the tale of Johann Beringer, a professor in 1725 who was made a fool when two of his colleagues planted fake fossils for him to find and research. Fortunately, this was the only fakery of the day.
The symposium began with opening remarks by Kirk Johnson, Sant Director of the National Museum of Natural History and Laurence Dorr, Chair of the Department of Botany. Johnson was pleased with the theme of the symposium this year, as the symposium coincides with the development of the Natural History Museum’s Deep Time exhibition, a major overhaul of the National Fossil Hall, which is scheduled to open to the public in June 2019.
Before the speakers’ talks began, Kenneth Wurdack presented the José Cuatrecasas Medal for Excellence in Tropical Botany to Alan Graham, a paleobotanist from the Missouri Botanical Garden. Graham recalled his time as a postdoctoral fellow at Harvard University and his “first social responsibility” in hosting a dinner for José Cuatrecasas and his wife. He was honored to be able to do that then, and now 56 years later, thrilled to be receiving an award in Cuatrecasas’ name.
Sir Peter Crane opened the symposium with a talk on the origin of flowering plants called “The Enigmatic ‘Mesozoic Seed Ferns.’” He introduced the complexity of studying the topic by discussing how the field of paleobotany has changed in recent decades. In the 1970s, paleobotany was a field that was literally frozen in stone due to a lack of high-quality fossils and tools to study them. Sir Peter demonstrated how far the field has come when he showed a digital reconstruction of a fossilized flower “bloom” for the crowd. Technology such as this allows scientists to study internal structures of fossilized plants.
Having demonstrated the advantages conferred by recent advances in technology and their impact on paleobotanical research, Sir Peter launched into his updated theory on seed ferns. He presented a new understanding of the origin of angiosperms based on his research of fossils collected from the Early Cretaceous in Mongolia. He explained that the origin of the outer integument and the carpel are two key questions for understanding the origin of angiosperms. He argued that the curvature responsible for the second integument in angiosperms has deep evolutionary roots. He explained that the origins of this curvature could be seen in diverse seed plants of the Mesozoic, such as Caytonia, corystosperms, and similar plants. Curvature results from the curvature of a seed-bearing axis that sometimes also bears modified bracts. Sir Peter explained that in pre-angiosperm seed plants, this curvature might be associated with a flotation based pollination mechanism involving saccate pollen, which appears to be basic in all but the very earliest diverging seed plant lineages. He concluded that many of the seed-plant lineages we now treat as independent may be closely allied.
The next speaker was Andrew Leslie, who gave a talk on the evolution of cones called “Biotic Seed Dispersal, Growth Architecture, and the Evolution of Conifer Cone Diversity.” He hypothesized what the first cones may have looked like, and why present cones look like the often spiky objects we are familiar with today. By examining the fossil record, Leslie was able to determine that proto-cones were modified shoots. The evolution of woodiness in long, thin, seemingly flexible cones was adaptively advantageous because it provided protection to their seeds from ever-evolving predators.
This discovery made Leslie question why small, fleshy, almost berry-like cones found in Cupressaceae and Podocarpaceae exist today. Unlike large, woody cones, the fossil record for these was scarce, and if any fossils did exist, they looked like “a black smudge within another black smudge that used to be a seed.” To work around this problem, Leslie developed a mathematical model that hypothesized transition rates between four cone types that could have existed: large, woody cones; small, woody cones; large, fleshy cones; and small, fleshy cones. After striking out large fleshy cones as a possibility, Leslie examined the model. This model helped him theorize that a cone’s morphology was dependent on the form of its tree’s branches and how animals dispersed its seeds. A tree with small branches would not grow large cones, and a tree with thick branches would not develop fleshy cones.
In his talk, “Ecophysiology of Extinct Plants,” Jonathan Wilson explained that the plant life we see today is a consequence of several hundred million years of evolution in response to the environment. Wilson told us that plants and their environments coevolved and each could tell us about the other. He advocated study of extinct plants as whole plants, rather than as disconnected fossil leaves or stems. He demonstrated that plants are integrated systems, and he used the example of a plant’s water transportation (what he calls the key to plant physiology) in his discussion. Plants are essentially composed of tubes; if we study how water was transported around a plant and where to, it will tell us which parts of the plant were most important to its survival and how humid or dry its environment was.
Wilson explained that the first vascular plants were experimenting with vascular tissue. He introduced the audience to the three plants with unusual structure: the Paleozoic “seed fern” Medullosa (large leaves on small stems; xylem cells that are among the largest in the fossil record), the Carboniferous tree fern Psaronius (root mantle surrounds stem), and the climbing sphenophyte Sphenophyllum (climbing hooks on heterophyllous leaves). He argued that within the Carboniferous ecosystems, plants occupied both ends of the modern hydraulic spectrum: high water transport efficiency but unsafe (Medullosa, Sphenophyllum) and lower water transport efficiency with higher safety margins (Psaronius, Cordaites). He concluded that plants have evolved a wide range of ecophysiological strategies over the last 400 million years, including “extinct ecophysiologies” that are not represented in extant ecosystems. Functioning of late Paleozoic tropical plants was more dynamic than inferred from phylogenetic relationships and it included the capability to force vegetation-climate feedbacks.
The afternoon session began with lectures on fossilized pollen and technology. The first was given by Surangi Punyasena on “Laying the Foundations for Automated Pollen Analysis,” and focused on her lab's development of machine-learning artificial intelligence (AI), which had been applied to the recognition and cataloguing of fossilized pollen in microscopic images. She used a labor-intensive method to create a virtual 3D-image of pollen samples, tagged data on each of the pollen grains, and then fed these into a neural net. This was the starting point for teaching her machine how to become a pollen expert. Punyasena's early tests have been running well, but she said that more data is needed to train the machine before it can reliably identify more complex pollen and beat trained humans. This new tool is exciting because it will be able to plow through large samples more quickly, and even identify broken, poorly preserved grains. Punyasena expanded the crowd's idea of what is possible in paleobotany, from the sepia-tinged field of a hundred years ago, to one moving into the gleaming era of AIs and neural nets.
Continuing the topic of technology, Selena Y. Smith gave a lecture on “Plant Paleobiology in the Digital Era: How X-Ray MicroCT is Helping to Shed Light on the History of Plants.” Smith spoke about the powerful ability of industrial X-ray micro-computed tomography (microCT) scans to reconstruct otherwise fragile or damaged fossils without doing further harm to museum specimens. Smith illustrated the usefulness of this technology through the example of a walnut. Using traditional investigative methods to identify an unknown walnut seed preserved in a slab of rock, a researcher would need to find part of a shell, an outer husk, the seed itself, or be unable to extract and examine the specimen without destroying it. Each part has the potential to be seen as a different plant. With microCT, a broken and apparently blank rock could be scanned, rejoined, and the seeds within rotated and examined from any angle.
Smith presented a case study of the evolutionary history of the Zingiberales. She described a project that analyzes 50 seed characters of over 200 specimens of Zingiberales using both traditional light microscopy as well as synchrotron-based tomography. The use of synchrotron tomography allowed her to reexamine non-destructively many rare and endangered extant taxa and fossils for study. One result that she discussed was the discovery that two species of fossil Alpinia were actually three species of Carpolithus and one species of Caricoidea (Cyperaceae). She concluded that non-destructive X-ray tomography is a powerful tool for fossil and modern plant material. A future goal is to build large comparative anatomical and morphological datasets to evaluate fossil affinities, reconstruct past environments, and provide calibration points with more confidence.
The theme of the next talk alternated away from tools of the trade to research, with Mónica Ramírez-Carvalho's lecture on “Late Cretaceous Floras from Northern South America and the Evolution of Neotropical Rainforests.” Carvalho collected fossils from Guajira, Colombia, at the site of the oldest known Neotropical rainforest (58-60 Ma) – now one of the largest open pit coal mines in the world. She examined these fossils to learn more about what Neotropical rainforests looked like before the Cretaceous–Paleogene (K/Pg) extinction event. Carvalho cataloged plant types, examined fossils of leaves for evidence of insects, and identified pollen remains. She found high abundance of leaf damage, low species diversity, and the same family-level composition as in Neotropical forests of today.
Carvalho asked what pre-Paleocene tropical forests were like and how Neotropical forests changed throughout the Cenozoic. A study of 800 leaf samples plus 350 new collections shows that the pattern of family-level dominance in pre-extinction times (~70 Ma) was different from the late Paleocene. She also discovered that leaf damage diversity is notably higher in the Cretaceous floras. Over the next few years, Carvalho will be conducting experiments in temperature- and CO2-controlled greenhouses at the Smithsonian Tropical Research Institute that test hypotheses related to dramatic environmental changes, such as the hyperthermals of the Early Eocene. The objectives of her study will be to test for increased evapotranspiration under high CO2 and high temperature.
The last lecture of the day was given by Susana Magallón on “The Different Roles of Fossils for Time-Calibrating Phylogenies.” This talk focused on tools and methods that are used to estimate divergence times, with a special focus on flowering plants. She presented three objectives of her talk: the type of data used in the models, the specific role of fossils, and examples from studies that estimate the age of crown group angiosperms. She then presented five different methods that are used to estimate divergence times. The first two methods estimate diversity times by excluding the fossil record (for example, using amino acid sequence data of cytochrome C in different plant species) and by only using the fossil record (for example, using plant macrofossil records at the genus level). These two models give a divergence time estimate of angiosperms at 230-310 Ma and 133-152 Ma, respectively.
The next three methods to estimate divergence times involve a relaxed molecular clock, which allows the molecular rate to vary among lineages. One method uses fossils to calibrate phylogenetic nodes, the oldest discovered representative of the clade. Another uses fossils as phylogenetic terminals, in which fossils are treated as taxa and placed on the tips of the tree. The last uses fossils as part of the phylogeny-generating model and of the diversification process, in which fossils are represented either as tips or ancestors. Also called the fossilized birth-death process, this final method gives a divergence time estimate of 150-182 Ma. Magallón’s research will be important for future studies involving the timeline of plant evolution and diversification and other studies involving deep time dating.
th Smithsonian Botanical Symposium is scheduled to return to Baird Auditorium at the National Museum of Natural History on Friday, 17 May 2019. The theme will be structured around the topic of domestication of plants. Check the symposium website <https://botany.si.edu/sbs> for updates.