Kathleen M. Pryer

A classification for extant ferns

We present a revised classification for extant ferns, with emphasis on ordinal and familial ranks, and a synopsis of included genera. Our classification reflects recently published phylogenetic hypotheses based on both morphological and molecular data. Within our new classification, we recognize four monophyletic classes, 11 monophyletic orders, and 37 families, 32 of which are strongly supported as monophyletic. One new family, Cibotiaceae Korall, is described. The phylogenetic affinities of a few genera in the order Polypodiales are unclear and their familial placements are therefore tentative. Alphabetical lists of accepted genera (including common synonyms), families, orders, and taxa of higher rank are provided.

Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis

Small subunit rRNA sequence data were generated for 27 strains of cyanobacteria and incorporated into a phylogenetic analysis of 1,377 aligned sequence positions from a diverse sampling of 53 cyanobacteria and 10 photosynthetic plastids. Tree inference was carried out using a maximum likelihood method with correction for site‐to‐site variation in evolutionary rate. Confidence in the inferred phylogenetic relationships was determined by construction of a majority‐rule consensus tree based on alternative topologies not considered to be statistically significantly different from the optimal tree. The results are in agreement with earlier studies in the assignment of individual taxa to specific sequence groups. Several relationships not previously noted among sequence groups are indicated, whereas other relationships previously supported are contradicted. All plastids cluster as a strongly supported monophyletic group arising near the root of the cyanobacterial line of descent.

Ferns diversified in the shadow of angiosperms

The rise of angiosperms during the Cretaceous period is often portrayed as coincident with a dramatic drop in the diversity and abundance of many seed-free vascular plant lineages, including ferns. This has led to the widespread belief that ferns, once a principal component of terrestrial ecosystems, succumbed to the ecological predominance of angiosperms and are mostly evolutionary holdovers from the late Palaeozoic/early Mesozoic era. The first appearance of many modern fern genera in the early Tertiary fossil record implies another evolutionary scenario; that is, that the majority of living ferns resulted from a more recent diversification. But a full understanding of trends in fern diversification and evolution using only palaeobotanical evidence is hindered by the poor taxonomic resolution of the fern fossil record in the Cretaceous. Here we report divergence time estimates for ferns and angiosperms based on molecular data, with constraints from a reassessment of the fossil record. We show that polypod ferns (> 80% of living fern species) diversified in the Cretaceous, after angiosperms, suggesting perhaps an ecological opportunistic response to the diversification of angiosperms, as angiosperms came to dominate terrestrial ecosystems.

Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants

Most of the 470-million-year history of plants on land belongs to bryophytes, pteridophytes and gymnosperms, which eventually yielded to the ecological dominance by angiosperms 90 Myr ago. Our knowledge of angiosperm phylogeny, particularly the branching order of the earliest lineages, has recently been increased by the concurrence of multigene sequence analyses. However, reconstructing relationships for all the main lineages of vascular plants that diverged since the Devonian period has remained a challenge. Here we report phylogenetic analyses of combined data—from morphology and from four genes—for 35 representatives from all the main lineages of land plants. We show that there are three monophyletic groups of extant vascular plants: (1) lycophytes, (2) seed plants and (3) a clade including equisetophytes (horsetails), psilotophytes (whisk ferns) and all eusporangiate and leptosporangiate ferns. Our maximum-likelihood analysis shows unambiguously that horsetails and ferns together are the closest relatives to seed plants. This refutes the prevailing view that horsetails and ferns are transitional evolutionary grades between bryophytes and seed plants, and has important implications for our understanding of the development and evolution of plants.

Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes

In an effort to obtain a solid and balanced approximation of global fern phylogeny to serve as a tool for addressing large-scale evolutionary questions, we assembled and analyzed the most inclusive molecular dataset for leptosporangiate ferns to date. Three plastid genes (rbcL, atpB, atpA), totaling more than 4,000 bp, were sequenced for each of 400 leptosporangiate fern species (selected using a proportional sampling approach) and five outgroups. Maximum likelihood analysis of these data yielded an especially robust phylogeny: 80% of the nodes were supported by a maximum likelihood bootstrap percentage ≥ 70. The scope of our analysis provides unprecedented insight into overall fern relationships, not only delivering additional support for the deepest leptosporangiate divergences, but also uncovering the composition of more recently emerging clades and their relationships to one another.

Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy

In todays angiosperm-dominated terrestrial ecosystems, leptosporangiate ferns are truly exceptional—accounting for 80% of the ≈11,000 nonflowering vascular plant species. Recent studies have shown that this remarkable diversity is mostly the result of a major leptosporangiate radiation beginning in the Cretaceous, following the rise of angiosperms. This pattern is suggestive of an ecological opportunistic response, with the proliferation of flowering plants across the landscape resulting in the formation of many new niches—both on forest floors and within forest canopies—into which leptosporangiate ferns could diversify. At present, one-third of leptosporangiate species grow as epiphytes in the canopies of angiosperm-dominated tropical rain forests. However, we know too little about the evolutionary history of epiphytic ferns to assess whether or not their diversification was in fact linked to the establishment of these forests, as would be predicted by the ecological opportunistic response hypothesis. Here we provide new insight into leptosporangiate diversification and the evolution of epiphytism by integrating a 400-taxon molecular dataset with an expanded set of fossil age constraints. We find evidence for a burst of fern diversification in the Cenozoic, apparently driven by the evolution of epiphytism. Whether this explosive radiation was triggered simply by the establishment of modern angiosperm-dominated tropical rain forest canopies, or spurred on by some other large-scale extrinsic factor (e.g., climate change) remains to be determined. In either case, it is clear that in both the Cretaceous and Cenozoic, leptosporangiate ferns were adept at exploiting newly created niches in angiosperm-dominated ecosystems.

Phylogenetic Relationships and Evolution of Extant Horsetails, Equisetum, Based on Chloroplast DNA Sequence Data (rbcL and trnL‐F)

Equisetum is a small and morphologically distinct genus with a rich fossil record. Two subgenera have been recognized based principally on stomatal position and stem branching: subg. Equisetum (eight species; superficial stomates; stems branched) and subg. Hippochaete (seven species; sunken stomates; stems generally unbranched). Prior attempts at understanding Equisetum systematics, phylogeny, and character evolution have been hampered by the high degree of morphological plasticity in the genus as well as by frequent hybridization among members within each subgenus. We present the first explicit phylogenetic study of Equisetum, including all 15 species and two samples of one widespread hybrid, Equisetum ×ferrissii, based on a combined analysis of two chloroplast markers, rbcL and trnL‐F. Our robustly supported phylogeny identifies two monophyletic clades corresponding to the two subgenera recognized by earlier workers. The phylogenetic placement of Equisetum bogotense, however, is ambiguous. In maximum likelihood analyses, it allies with subg. Hippochaete as the most basal member, while maximum parsimony places it as sister to the rest of the genus. A consensus phylogeny from the two analyses is presented as a basal trichotomy (E. bogotense, subg. Hippochaete, subg. Equisetum), and morphological character evolution is discussed. We detected rate heterogeneity in the rbcL locus between the two subgenera that can be attributed to an increased rate of nucleotide substitution (transversions) in subg. Hippochaete. We calculated molecular‐based age estimates using the penalized likelihood approach, which accounts for rate heterogeneity and does not assume a molecular clock. The Equisetum crown group appears to have diversified in the early Cenozoic, whereas the Equisetaceae total group is estimated to have a Paleozoic origin. These molecular‐based age estimates are in remarkable agreement with current interpretations of the fossil record.

Plastid atpA data provide improved support for deep relationships among ferns

DNA sequence data and phylogenetic approaches have contributed greatly to our understanding of fern relationships. Nonetheless, the datasets analyzed to date have not been sufficient to definitively resolve all parts of the global fern phylogeny; additional data and more extensive sampling are necessary. Here, we explore the phylogenetic utility of the plastid atpA gene. Using newly designed primers, we obtained atpA sequences for 52 fern and 6 outgroup taxa, and then evaluated the capabilities of atpA relative to four other molecular markers, as well as the contributions of atpA in combined analyses. The five single-gene datasets differed markedly in the number of variable characters they possessed; and although the relationships resolved in analyses of these datasets were largely congruent, the robustness of the hypotheses varied considerably. The atpA dataset had more variable characters and resulted in a more robustly supported phylogeny than any of the other single gene datasets examined, suggesting that atpA will be exceptionally useful in more extensive studies of fern phylogeny and perhaps also in studies of other plant lineages. When the atpA data were analyzed in combination with the other four markers, an especially robust hypothesis of fern relationships emerged. With the addition of the atpA data, support increased substantially at several nodes; three nodes, which were not well-supported previously, received both good posterior probability and good bootstrap support in the combined 5-gene (> 6 kb) analyses.

Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns

Significance Despite being one of the oldest groups of land plants, the majority of living ferns resulted from a relatively recent diversification following the rise of angiosperms. To exploit fully the new habitats created by angiosperm-dominated ecosystems, ferns had to evolve novel adaptive strategies to cope with the low-light conditions exerted by the angiosperm canopy. Neochrome, an unconventional photoreceptor that allows ferns to “see the light” better, was likely part of the solution. Surprisingly, we discovered that fern neochrome was derived from a bryophyte lineage via horizontal gene transfer (HGT). This finding not only provides the first evidence that a plant-to-plant HGT can have a profound evolutionary impact but also has implications for the evolution of photosensory systems in plants. Ferns are well known for their shade-dwelling habits. Their ability to thrive under low-light conditions has been linked to the evolution of a novel chimeric photoreceptor—neochrome—that fuses red-sensing phytochrome and blue-sensing phototropin modules into a single gene, thereby optimizing phototropic responses. Despite being implicated in facilitating the diversification of modern ferns, the origin of neochrome has remained a mystery. We present evidence for neochrome in hornworts (a bryophyte lineage) and demonstrate that ferns acquired neochrome from hornworts via horizontal gene transfer (HGT). Fern neochromes are nested within hornwort neochromes in our large-scale phylogenetic reconstructions of phototropin and phytochrome gene families. Divergence date estimates further support the HGT hypothesis, with fern and hornwort neochromes diverging 179 Mya, long after the split between the two plant lineages (at least 400 Mya). By analyzing the draft genome of the hornwort Anthoceros punctatus, we also discovered a previously unidentified phototropin gene that likely represents the ancestral lineage of the neochrome phototropin module. Thus, a neochrome originating in hornworts was transferred horizontally to ferns, where it may have played a significant role in the diversification of modern ferns.

A molecular phylogeny of scaly tree ferns (Cyatheaceae)

Tree ferns recently were identified as the closest sister group to the hyperdiverse clade of ferns, the polypods. Although most of the 600 species of tree ferns are arborescent, the group encompasses a wide range of morphological variability, from diminutive members to the giant scaly tree ferns, Cyatheaceae. This well-known family comprises most of the tree fern diversity (∼500 species) and is widespread in tropical, subtropical, and south temperate regions of the world. Here we investigate the phylogenetic relationships of scaly tree ferns based on DNA sequence data from five plastid regions (rbcL, rbcL-accD IGS, rbcL-atpB IGS, trnG-trnR, and trnL-trnF). A basal dichotomy resolves Sphaeropteris as sister to all other taxa and scale features support these two clades: Sphaeropteris has conform scales, whereas all other taxa have marginate scales. The marginate-scaled clade consists of a basal trichotomy, with the three groups here termed (1) Cyathea (including Cnemidaria, Hymenophyllopsis, Trichipteris), (2) Alsophila sensu stricto, and (3) Gymnosphaera (previously recognized as a section within Alsophila) + A. capensis. Scaly tree ferns display a wide range of indusial structures, and although indusium shape is homoplastic it does contain useful phylogenetic information that supports some of the larger clades recognised.