Early Trait Evolution in Liverworts (Marchantiophyta), with an emphasis on Oil Bodies and Paleozoic Taxa
Susan Lorraine Tremblay
Doctor of Philosophy in Integrative Biology
University of California, Berkeley
Professor Brent D. Mishler, Chair
Liverworts (Marchantiophyta) are a diverse and phylogenetically important group of land plants (Embryophytes). They diverged early on from the rest of the land plants, but few fossils exist from the Paleozoic or Mesozoic and those that do exist generally possess only a few vegetative characters. By the Cenozoic, when liverwort fossils become more common, modern groups had evolved and the fossils can be easily placed. Consequently little is known about early character evolution in liverworts. Recently, studies based on molecular data have resolved the liverwort phylogeny, and together with new fossil discoveries they offer an opportunity to reassess the early evolution of liverworts.
One of the most important liverwort characters are the unique organelles found in most of their cells called oil bodies. Considered a synapomorphy of liverworts, oil bodies are bound by a biological membrane and synthesize and sequester a wide variety of terpenoids and aromatic compounds, yet their exact role in the cell is not known. They can easily be observed through a light microscopy and are taxonomically informative. The first chapter of this thesis reviews what is known about oil bodies from a phylogenetic perspective. Structure and chemistry of oil bodies is reviewed, with special attention to assignment of oil body 'types' to groups based on the recent classification of liverworts.
Hypotheses of oil body evolution generally assume an ancestor with a single type of oil body, with the present diversity of oil bodies having evolved from the ancestral type. As documented in this review, similar variation in oil body types occurs in distantly related clades across the newly resolve phylogeny, including the earliest diverging groups, suggesting that the most recent common ancestor of the group may have been polymorphic for oil body types. Some liverwort taxa have secondarily lost oil bodies. Comparing these taxa to their sister groups could offer insight into oil body function. Some experimental evidence supports the anti-herbivory hypothesis of oil body function. Hypotheses of oil body evolution and oil body function need to be tested using both systematic and ecological methods.
In some groups oil bodies occur only in special, scattered cells that contain one large oil body. In my second chapter I test the hypothesized homology of the dark scattered cells of some Paleozoic liverwort fossils with the specialized oil body cells of some modern liverwort taxa. Fresh fossils of the oldest known liverwort, the recently discovered Metzgeriothallus sharonae Hernick, were collected and isolated from the matrix and their cells were compared to those of modern taxa using light microscopy, scanning electron microscopy, and fluorescence microscopy. Frequency of occurrence and area coverage of the dark cells were compared to several modern taxa. All results support the homology of the fossil dark cells and modern oil body cells, providing an important new character for use in assigning fossils to the liverworts and potentially to specific groups. It will also help elucidate the plesiomorphic state of liverwort oil bodies. The results showed that the dark cells of M. sharonae are more numerous near thallus margins providing circumstantial evidence for the anti-herbivory hypothesis of their function.
Metzgeriothallus sharonae is spectacularly preserved in situ and the acid maceration revealed complex branching previously unknown in Paleozoic liverworts. While M. sharonae was the dominant plant in the assemblage, similarly well-preserved organic remains of dozens of co-existing organisms were also recovered. In the third chapter of this thesis I describe these new features and the community these ancient liverworts were a dominant member of. The dimorphic structure of the plants, broad, dichotomizing thalli alternating with narrower, twisting thalli that have many intercalary branches suggests the plants were growing both above and below the surface of and along banks of shallow pools. Metzgeriothallus sharonae is the only Paleozoic thalloid liverwort to exhibit intercalary branching as well as ventral branching at the thallus apex. The Cairo Quarry liverwort lens represents a conservation lagerstatte, a miniature 'frozen' freshwater ecosystem that is the only known liverwort dominated community from the Paleozoic.