Paul Kenrick

The origin and early evolution of plants on land

The origin and early evolution of land plants in the mid-Palaeozoic era, between about 480 and 360 million years ago, was an important event in the history of life, with far-reaching consequences for the evolution of terrestrial organisms and global environments. A recent surge of interest, catalysed by palaeobotanical discoveries and advances in the systematics of living plants, provides a revised perspective on the evolution of early land plants and suggests new directions for future research.

A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic

The geochemical carbon cycle is strongly influenced by life on land, principally through the effects of carbon sequestration and the weathering of calcium and magnesium silicates in surface rocks and soils. Knowing the time of origin of land plants and animals and also of key organ systems (e.g. plant vasculature, roots, wood) is crucial to understand the development of the carbon cycle and its effects on other Earth systems. Here, we compare evidence from fossils with calibrated molecular phylogenetic trees (timetrees) of living plants and arthropods. We show that different perspectives conflict in terms of the relative timing of events, the organisms involved and the pattern of diversification of various groups. Focusing on the fossil record, we highlight a number of key biases that underpin some of these conflicts, the most pervasive and far-reaching being the extent and nature of major facies changes in the rock record. These effects probably mask an earlier origin of life on land than is evident from certain classes of fossil data. If correct, this would have major implications in understanding the carbon cycle during the Early Palaeozoic.

Phylogeny of Lycopodiaceae (Lycopsida) and the Relationships of Phylloglossum drummondii Kunze Based on rbcL Sequences

A cladistic analysis based on rbcL sequences from a representative sample of 12 species yields a single most parsimonious tree that supports monophyly of Lycopodiaceae, Lycopodium, and Lycopodiella. Huperzia is resolved as paraphyletic to the morphologically divergent, monotypic Australasian Phylloglossum. The Huperzia-Phylloglossum clade is strongly supported and is sister group to a Lycopodium-Lycopodiella clade. These results provide the first clear evidence for the relationships of the problematic Phylloglossum drummondii. Profound differences in life cycle and morphology between Phylloglossum and other Lycopodiaceae are interpreted in terms of pedomorphosis (specifically, progenesis) and are viewed as adaptive responses to drought and brush fire. Our results show that rbcL sequence divergence among neotropical species of the supposedly ancient genus Huperzia is extremely low and that additional data will be necessary to resolve relationships among epiphytes and ground-living species. These surprisingly low levels of sequence divergence indicate that most living species diversity within Lycopodiaceae is of relatively recent origin Our results are consistent with a late Cretaceous or early Tertiary origin and diversification of epiphytic species within Huperzia, and these events may be linked to the diversification of angiosperms.

PHYLOGENETIC RELATIONSHIPS IN SELAGINELLACEAE BASED ON RBCL SEQUENCES

A phylogenetic framework is developed for the clubmoss family Selaginellaceae based on maximum parsimony analyses of molecular data. The chloroplast gene rbcL was sequenced for 62 species, which represent nearly 10% of living species diversity in the family. Taxa were chosen to reflect morphological, geographical, and ecological diversity. The analyses provide support for monophyly of subgenera Selaginella and Tetragonostachys. Stachygynandrum and Heterostachys are polyphyletic. Monophyly of Ericetorum is uncertain. Results also indicate a large number of new groupings not previously recognized on morphological grounds. Some of these new groups seem to have corresponding morphological synapomorphies, such as the presence of rhizophores (distinctive root-like structures), aspects of rhizophore development, and leaf and stem morphology. Others share distinctive ecological traits (e.g., xerophytism). For many groups, however, no morphological, ecological, or physiological markers are known. This could reflect patchy sampling and a lack of detailed knowledge about many species. Despite a lengthy fossil record dating from the Carboniferous Period, cladogram topology indicates that most of the living tropical species are probably the products of more recent diversifications. Resurrection plants, extreme xerophytes characterized by aridity-driven inrolling of branches and rapid revival on rehydration, have evolved at least three times in quite different clades.

Epiphytism and terrestrialization in tropicalHuperzia (Lycopodiaceae)

A phylogenetic analysis ofHuperzia (Lycopodiaceae) documents a single origin of epiphytism and multiple reversals to a terrestrial habit in the Neotropics. Epiphytism evolved prior to the final rifting of South America and Africa, but the origin of most modern species diversity probably postdates the Mid Cretaceous diversification of flowering plants. In this respect, the evolution ofHuperzia parallels that of many other Neotropical epiphytic groups. In the Andes, alpine terrestrial species are shown to have evolved from montane epiphytes, an event that correlates well with regional orogenesis during the Miocene. Species from Australia, New Zealand, and Tasmania show diverse relationships with SE Asian groups. Results also indicate that long distance, transoceanic dispersal is rare in these homosporous plants — accounting for less than 5% of species distributions — and that convergence in strobilus and branch morphology is widespread among Paleotropical and Neotropical epiphytes. The phylogenetic analysis is based on a sample of 63 species (c. 15% total species diversity) and data from a c. 1.1kb region of noncoding (intron and spacer sequences) plastid DNA located between thetrnL andtrnF genes.

The origin and early evolution of roots

Exceptionally well-preserved fossils shed light on the earliest roots and their interactions with the environment. Geological sites of exceptional fossil preservation are becoming a focus of research on root evolution because they retain edaphic and ecological context, and the remains of plant soft tissues are preserved in some. New information is emerging on the origins of rooting systems, their interactions with fungi, and their nature and diversity in the earliest forest ecosystems. Remarkably well-preserved fossils prove that mycorrhizal symbionts were diverse in simple rhizoid-based systems. Roots evolved in a piecemeal fashion and independently in several major clades through the Devonian Period (416 to 360 million years ago), rapidly extending functionality and complexity. Evidence from extinct arborescent clades indicates that polar auxin transport was recruited independently in several to regulate wood and root development. The broader impact of root evolution on the geochemical carbon cycle is a developing area and one in which the interests of the plant physiologist intersect with those of the geochemist.

Palaeontology. Turning over a new leaf.

A model based on biophysical principles of plant physiology, and drawing on fossil and environmental data, indicates that the origin of leaves was triggered by falling levels of atmospheric CO2.

DIVERTED DEVELOPMENT OF REPRODUCTIVE ORGANS : A SOURCE OF MORPHOLOGICAL INNOVATION IN LAND PLANTS

Recent discussions of animal development, particularly at the level of molecular genetics, have emphasized modularity, dissociation and co-option as basic principles of evolutionary developmental biology. These concepts are discussed in relation to two specific structural innovations in land plant evolution: the leaves (microphylls) of lycopsids, and the interseminal scales ofBennettitales. Both structures appear to have been derived evolutionarily by the diverted development of reproductive organs. In the case of lycopsids, recent analyses of phylogenetic relationships suggest that leaves are sterilized sporangia modified for photosynthetic assimilation. In the case ofBennettitales, structural data suggest that the interseminal scales are sterilized “cupules” modified for protection of the ovules. In both cases, multiplication of reproductive organs seems to have accentuated functional redundancy, and together with the developmental autonomy (dissociation) already inherent in the modular construction of plants, appears to have facilitated sterilization and co-option of some of these structures for new purposes. Numerous other examples in plants illustrate the same principles.

Schizaeaceae: a phylogenetic approach

Schizaeaceae fossils have been documented throughout Mesozoic and Cenozoic deposits, but our understanding of this fossil record is hampered by uncertainties with respect to the relationships of living species. To start building a phylogenetic framework for the family, an initial phylogenetic analysis of living species using plastid rbcL nucleotide sequence data is conducted. The analysis supports Schizaea s. lat. and Lygodium monophyly, but Anemia is resolved as paraphyletic to Mohria. In the Anemia/Mohria clade, monophyly of subgenus Anemiorrhiza is supported, but Coptophyllum is resolved as paraphyletic to subgenus Anemia. In Schizaea s. lat., both Schizaea s. str. and Actinostachys are well supported and Microschizaea is grouped with Schizaea s. str., although only one Microschizaea species (Schizaea pusilla) was included. These results are largely congruent with previous morphology-based analyses. In Lygodium however, results presented contrast with recent morphological analyses highlighting the problems of identifying Lygodium subgeneric groups. Using the resulting phylogeny as a framework, putative relationships of fossil species are discussed, tentative minimum age estimates for generic crown group diversifications are made, and possible conclusions with respect to the origins of habit and habitat preferences are discussed. The fossil evidence indicates that subgeneric groups within the Anemia/Mohria clade are comparatively ancient, originating during the Early Cretaceous, and the putative placement of fossil Anemia within the crown group of living subgenus Anemiorrhiza would indicate that their calcareous habitat preference may be a relic feature that has persisted ever since the Early Cretaceous. Lygodium on the other hand appears to have passed through a diversity bottleneck. Modern species diversity probably originated in the Neogene, and the earliest fossil evidence for the origin of their vining and trailing habit comes from the placement of Miocene fossil Lygodium within the crown group of living species.

Phylogeny of Selaginellaceae: Evaluation of Generic/Subgeneric Relationships Based on rbcL Gene Sequences

A cladistic analysis based on rbcL gene sequences from a representative sample of 18 species yields three most parsimonious trees that strongly support monophyly of Selaginellaceae. Within Selaginellaceae, the morphologically distinctive subgenus Selaginella is resolved as sister group to a clade composed of all other species, here termed the rhizophoric clade. In the rhizophoric clade, subgenus Stachygynandrum is paraphyletic to subgenera Ericetorum, Tetragonostachys, and Heterostachys. Monophyly of Ericetorum and Tetragonostachys is strongly corroborated. Results support a close relationship between “resurrection plants” in Stachygynandrum and the mat‐forming or tufted drought‐tolerant species of Tetragonostachys, indicating a common origin of xerophytism in these groups. A close relationship for all isophyllous species, as hypothesized in many classifications, is not supported by the rbcL data. Leaf isophylly and reduction in Ericetorum and Tetragonostachys most probably represent independent reversals of the marked anisophyllous condition in Stachygynandrum. Leaf reduction is one of a suite of characters that may have evolved in response to seasonal drought.