Michael Sundue

A community-derived classification for extant lycophytes and ferns

Phylogeny has long informed pteridophyte classification. As our ability to infer evolutionary trees has improved, classifications aimed at recognizing natural groups have become increasingly predictive and stable. Here, we provide a modern, comprehensive classification for lycophytes and ferns, down to the genus level, utilizing a community‐based approach. We use monophyly as the primary criterion for the recognition of taxa, but also aim to preserve existing taxa and circumscriptions that are both widely accepted and consistent with our understanding of pteridophyte phylogeny. In total, this classification treats an estimated 11 916 species in 337 genera, 51 families, 14 orders, and two classes. This classification is not intended as the final word on lycophyte and fern taxonomy, but rather a summary statement of current hypotheses, derived from the best available data and shaped by those most familiar with the plants in question. We hope that it will serve as a resource for those wanting references to the recent literature on pteridophyte phylogeny and classification, a framework for guiding future investigations, and a stimulus to further discourse.

A 4000-species dataset provides new insight into the evolution of ferns

Ferns are the second-most diverse lineage of vascular plants on Earth, yet the best-sampled time-calibrated phylogeny of the group to date includes fewer than 5% of global diversity and was published seven years ago. We present a time-calibrated phylogeny that includes nearly half of extant fern diversity. Our results are evaluated in the context of previous studies and the fossil record, and we develop new hypotheses about the radiation of leptosporangiate ferns. We used sequence data from six chloroplast regions for nearly 4000 species of ferns to generate the most comprehensive phylogeny of the group ever published. We calibrate the phylogeny with twenty-six fossils and use an array of phylogenetic methods to resolve phylogenetic relationships, estimate divergence times, and infer speciation, extinction, and net diversification rates. We infer a mid-late Silurian origin for ferns (including horsetails) and an early Carboniferous origin for leptosporangiate ferns. Most derived fern families appeared in the Cretaceous and persisted for millions of years before rapidly diversifying in the Cenozoic. We find no evidence of differential rates of diversification among terrestrial and epiphytic species. Our findings challenge previous hypotheses on the evolutionary history of ferns and present a new paradigm for their Cenozoic radiation. We estimate earlier divergences for most fern lineages than were reported in previous studies and provide evidence of extended persistence of major fern lineages prior to rapid diversification in the last fifty million years.

Phylogeny and Character Evolution of the Bolbitidoid Ferns (Dryopteridaceae)

We performed a phylogenetic analysis of the traditionally recognized genera of bolbitidoid ferns (i.e., Arthrobotrya, Bolbitis, Elaphoglossum, Lomagramma, and Teratophyllum) using two noncoding chloroplast spacers: trnL‐trnF and rps4‐trnS. The sampling included 57 species, of which 55 had not been sequenced previously. The results supported the monophyly of bolbitidoid ferns and of Arthrobotrya, Elaphoglossum, Lomagramma, and Teratophyllum; however, Bolbitis was resolved as polyphyletic. A clade of eight Neotropical species currently placed in Bolbitis is sister to Elaphoglossum, not the other species of Bolbitis. We refer to this group of species as the Bolbitis nicotianifolia clade. Lomagramma (or Bolbitis) guianensis, whose generic placement has been uncertain, was found to belong to the B. nicotianifolia clade. Bolbitis s.s. was resolved sister to the rest of the bolbitidoid ferns, which are in turn divided into two clades, one consisting of Elaphoglossum and the B. nicotianifolia clade and the other of Lomagramma, Teratophyllum, and Arthrobotrya. We optimized 34 morphological characters on the resulting phylogenetic tree. The characters found to be synapomorphic for bolbitidoid ferns were ventral root insertion, elongated ventral meristeles, sterile‐fertile leaf dimorphism, acrostichoid sori, and the absence of hairs on the leaves. Other characters, such as articulate pinnae, venation patterns, laminar buds, paraphyses, and growth habit, are discussed in relation to the clades they support at different nodes on the tree. The bolbitidoid ferns show a transition series from terrestrial (Bolbitis) to hemiepiphytic (the B. nicotianifolia clade, Arthrobotrya, Lomagramma, and Teratophyllum) to epiphytic (Elaphoglossum). A sister‐species relationship between the Neotropical Bolbitis serratifolia and the African Bolbitis acrostichoides was recovered, supporting their relationship as previously postulated on the basis of morphology.

Systematics of Grammitid Ferns (Polypodiaceae): Using Morphology and Plastid Sequence Data to Resolve the Circumscriptions of Melpomene and the Polyphyletic Genera Lellingeria and Terpsichore

Abstract Recent phylogenetic analyses of grammitid ferns (Polypodiaceae) have demonstrated that some genera recognized within this clade are not monophyletic. We focus on resolving the circumscriptions of some large Neotropical genera by focusing on a clade, identified in previous analyses, that includes the monophyletic genus Melpomene, plus portions of two polyphyletic genera, Lellingeria and Terpsichore. Phylogenetic analyses using chloroplast markers atpB, rbcL, and trnL-F, along with 109 morphological characters, resolve this ingroup as monophyletic and sister to a clade that includes Ceradenia, Enterosora, and Zygophlebia. We use morphological characters included in the analysis to circumscribe clades. Melpomene is clearly monophyletic, but forms a polytomy with Lellingeria s. l. in a strict consensus of MP trees. Ingroup species of Terpsichore form three well supported monophyletic groups that together are paraphyletic with respect to Melpomene plus Lellingeria. Two clades corresponding to species groups of Terpsichore will be recognized as new genera.

Global phylogeny and biogeography of grammitid ferns (Polypodiaceae).

We examined the global historical biogeography of grammitid ferns (Polypodiaceae) within a phylogenetic context. We inferred phylogenetic relationships of 190 species representing 31 of the 33 currently recognized genera of grammitid ferns by analyzing DNA sequence variation of five plastid DNA regions. We estimated the ages of cladogenetic events on an inferred phylogeny using secondary fossil calibration points. Historical biogeographical patterns were inferred via ancestral area reconstruction. Our results supported four large-scale phylogenetic and biogeographic patterns: (1) a monophyletic grammitid clade that arose among Neotropical polypod ancestors about 31.4 Ma; (2) a paraphyletic assemblage of clades distributed in the Neotropics and the Afro-Malagasy region; (3) a large clade distributed throughout the Asia-Malesia-Pacific region that originated about 23.4 Ma; and, (4) an Australian or New Zealand origin of the circumaustral genus Notogrammitis. Most genera were supported as monophyletic except for Grammitis, Oreogrammitis, Radiogrammitis, and Zygophlebia. Grammitid ferns are a well-supported monophyletic group with two biogeographically distinct lineages: a primarily Neotropical grade exhibiting several independent successful colonizations to the Afro-Malagasy region and a primarily Paleotropical clade exhibiting multiple independent dispersals to remote Pacific islands and temperate, austral regions.

Molecular phylogeny, character evolution, and biogeography of the grammitid fern genus Lellingeria (Polypodiaceae)

UNLABELLED PREMISE OF THE STUDY The recognition of monophyletic genera for groups that have high levels of homoplastic morphological characters and/or conflicting results obtained by different studies can be difficult. Such is the case in the grammitid ferns, a clade within the Polypodiaceae. In this study, we aim to resolve relationships among four clades of grammitid ferns, which have been previously recovered either as a polytomy or with conflicting topologies, with the goal of circumscribing monophyletic genera. • METHODS The sampling included 89 specimens representing 61 species, and sequences were obtained for two genes (atpB and rbcL) and four intergenic spacers (atpB-rbcL, rps4-trnS, trnG-trnR, and trnL-trnF), resulting in a matrix of 5091 characters. The combined data set was analyzed using parsimony, likelihood, and Bayesian methods. Ninety-six morphological characters were optimized onto the generated trees, using the parsimony method. • KEY RESULTS Lellingeria is composed of two main clades, the L. myosuroides and the Lellingeria s.s. clades, which together are sister to Melpomene. Sister to all three of these is a clade with two species of the polyphyletic genus Terpsichore. In the L. myosuroides clade, several dispersal events occurred between the neotropics, Africa, and the Pacific Islands, whereas Lellingeria s.s. is restricted to the neotropics, with about 60% of its diversity in the Andes. • CONCLUSIONS Overall, our results suggest that Lellingeria is monophyletic, with two clades that are easily characterized morphologically and biogeographically. Morphological characters describing the indument are the most important to define the clades within the ingroup. A small clade, previously considered in Terpsichore, should be recognized as a new genus.

Morphological innovation, ecological opportunity, and the radiation of a major vascular epiphyte lineage

The emergence of angiosperm‐dominated tropical forests in the Cretaceous led to major shifts in the composition of biodiversity on Earth. Among these was the rise to prominence of epiphytic plant lineages, which today comprise an estimated one‐quarter of tropical vascular plant diversity. Among the most successful epiphytic groups is the Polypodiaceae, which comprises an estimated 1500 species and displays a remarkable breadth of morphological and ecological diversity. Using a time‐calibrated phylogeny for 417 species, we characterized macroevolutionary patterns in the family, identified shifts in diversification rate, and identified traits that are potential drivers of diversification. We find high diversification rates throughout the family, evidence for a radiation in a large clade of Paleotropical species, and support for increased rates of diversification associated with traits including chlorophyllous spores and noncordiform gametophytes. Contrary to previous hypotheses, our results indicate epiphytic species and groups with humus‐collecting leaves diversify at lower rates than the family as a whole. We find that diversification rates in the Polypodiaceae are positively correlated with changes in elevation. Repeated successful exploration of novel habitat types, rather than morphological innovation, appears to be the primary driver of diversification in this group.

A Morphological Cladistic Analysis of Terpsichore (Polypodiaceae)

Abstract Terpsichore, a Neotropical genus of about 70 species, was shown in previous molecular phylogenetic studies to be polyphyletic. The present study assesses this conclusion using morphology and also examines the phylogenetic relationships of five informal species groups originally described within Terpsichore. A morphological matrix was constructed for 109 qualitative characters and 129 terminals. Maximum parsimony was used to analyze the complete data set and three different partitions of that data set which excluded characters of either leaf shape or indumentum position or both. Terpsichore is polyphyletic in all analyses, and the characters originally used to define the genus are either plesiomorphic or homoplastic. Whereas the analysis of the complete matrix recovered a clade similar to the original circumscription, analyses of the partitioned data sets yielded results similar to those of molecular phylogenetic studies. In all analyses, two of the five infrageneric groups of Terpsichore are resolved as monophyletic, whereas the others are either paraphyletic or polyphyletic. In all analyses, species from the Terpsichore taxifolia Group are recovered as diphyletic, a result corresponding to that found in the previous molecular phylogenetic studies. By scoring morphological characters for this study, it was found that two vascular bundles are present in many grammitid petioles and are not unique to Luisma, mesophyll composed of long-armed stellate parenchyma evolves at least three times and is not unique to Enterosora, and perforated dictyosteles are common in grammitids and not restricted to Zygophlebia.

CRYPTOCHLOROPHYLLOUS SPORES IN FERNS: NONGREEN SPORES THAT CONTAIN CHLOROPHYLL

In terms of color, fern spores have traditionally been classified as either green or nongreen. This study reports a new kind of spore, here termed “cryptochlorophyllous.” Such spores contain chlorophyll but do not appear green when examined with either the naked eye or a light microscope. Epifluorescence microscopy was used to detect chlorophyll in cryptochlorophyllous spores. To test one aspect of the reliability of this method, we examined whether chlorophyll degradation over time would give false negative results. We found that in two species with green spores (Osmundastrum cinnamomeum and Terpsichore asplenifolia), fluorescence weakened with but could still be detected in specimens that were 110 yr old. We surveyed the spores of species in three fern genera under white light and with epifluorescence microscopy. Under white light, green spores were seen in 10 (26%) of 39 species of Elaphoglossum, two (17%) of 12 species of Lomariopsis, and seven (25%) of 28 species of Pleopeltis. When spores from the same species were examined with epifluorescence microscopy, fluorescence was detected in 22 (56%) of 39 species of Elaphoglossum, 10 (83%) of 12 species of Lomariopsis, and 12 (42%) of 28 species of Pleopeltis. We also found conflicting results in nine of the 33 species represented in our study by more than one specimen. In these species with conflicting results, at least one specimen fluoresced whereas the other(s) did not. The specimens that failed to fluoresce might have been collected and dried before the chloroplasts in its spores had developed, or they may represent infraspecific variation in this characteristic. Chlorophyll-containing spores have probably been overlooked in Elaphoglossum and Lomariopsis because the dark perispore obscures the green contents of the cell. In some species of Pleopeltis, such spores have probably been overlooked because of their paleness and the short duration of their greenness. Chlorophyll-containing spores are probably more widespread than is currently suspected, especially in clades known to contain both green and nongreen spores. Overall, the dichotomy of fern spores into green and nongreen is too simplistic. It must be investigated experimentally whether cryptochlorophyllous spores behave like visibly green spores in terms of germination and viability times.

New combinations in Lastreopsis and Parapolystichum (Dryopteridaceae)

Recent molecular phylogenetic studies have shown that Lastreopsis is paraphyletic. Twenty-seven of its species belong to a separate clade for which the previously published generic name Parapolystichum is available. Parapolystichum is widely distributed, with four species in the Neotropics, six in Africa, nine in Madagascar, and eight in Australia and New Zealand. We make the following 25 new combinations in Parapolystichum:P. acuminatum, P. acutum, P. barterianum, P. boivinii, P. confine, P. coriaceosquamatum, P. currorii subsp. currorii, P. currorii subsp. eglandulosum, P. excultum, P. fideleae, P. glabellum, P. hornei, P. manongarivense, P. microsorum ssp. microsorum, P. microsorum ssp. pentangulare, P. munitum, P. nigritianum, P. perrierianum, P. pseudoperrierianum, P. rufescens, P. smithianum, P. subsimile, P. tinarooense, P. vogelii, and P. windsorense. Also, we designate a lectotype for Dryopteris exculta var. squamifera (=Parapolystichum excultum). No known morphological characters distinguish Parapolystichum from Lastreopsis s.s. Certain species of Parapolystichum, however, bear buds distally along the rachis, whereas Lastreopsis lacks such buds. Because no morphological character, or suite of characters, consistently separates the two genera, nine species of Lastreopsis s.l., which were not included in the previous phylogenetic analyses, could not be classified in either Lastreopsis or Parapolystichum. New combinations are also made for L. dissecta, L. tripinnata and L. poecilophlebia, species previously classified in Oenotrichia and Coveniella. Because Coveniella was considered monotypic, it is here reduced to a synonym of Lastreopsis. As re-circumscribed here, Lastreopsis now consists of about 16 species, all restricted to southeastern Asia and Oceania.