Xian-Chun Zhang

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.

Phylogeography of the Sino-Himalayan Fern Lepisorus clathratus on “The Roof of the World”

Background The Qinghai-Tibetan Plateau (QTP) and its southern and southeastern mountain ranges, Himalaya-Hengduan Mountains (HHM), are one of the most extensive habitats for alpine plants in the world. How ferns occurring in QTP and HHM changed their distribution ranges in response to Quaternary climatic oscillations remains almost unknown. Methodology and Results We employed sequences of two chloroplast DNA regions, rps4-trnS and trnL-trnF, to reconstruct phylogeography of the Sino-Himalayan fern Lepisorus clathratus, occurring mainly in the QTP and HHM. Individuals of this species have either dehiscent or indehiscent sporangia with the latter evolved from the plesiomorphic dehiscent forms. Based on a range-wide sampling, we detected 27 cpDNA haplotypes that were divided into five groups by network analyses. Populations in the Hengduan Mountains possess the highest genetic diversity, while a single haplogroup is detected across the north-central region. A distinct phylogeographical subdivision was detected between the Hengduan Mountains and north-central region by AMOVA analysis. The haplogroup distribution pattern, coalescence and AMOVA analysis suggest that a long term survival area (refugia) of the species was located in the Hengduan Mountains during glaciations, with probable range expansions into north-central regions during interglacial periods. Populations with indehiscent sporangium can carry private haplotypes and are inclined to maintain genetic homogeneity. One group with indehiscent sporangia most likely survived in situ on the QTP during glaciations. Conclusions/Significance This study for the first time sheds light on the response of alpine ferns in the QTP and HHM to the Quaternary climatic oscillations.

The rise of the Himalaya enforced the diversification of SE Asian ferns by altering the monsoon regimes

BackgroundThe rise of high mountain chains is widely seen as one of the factors driving rapid diversification of land plants and the formation of biodiversity hotspots. Supporting evidence was reported for the impact of the rapid rise of the Andean mountains but this hypothesis has so far been less explored for the impact of the “roof of the world”. The formation of the Himalaya, and especially the rise of the Qinghai–Tibetan Plateau in the recent 20 million years, altered the monsoon regimes that dominate the current climates of South East Asia. Here, we infer the hypothesis that the rise of Himalaya had a strong impact on the plant diversity in the biodiversity hotspot of the Southwest Chinese Mountains.ResultsOur analyses of the diversification pattern of the derived fern genus Lepisorus recovered evidence for changes in plant diversity that correlated with the strengthening of South East Asian monsoon. Southwest China or Southwest China and Japan was recovered as the putative area of origin of Lepisorus and enhancing monsoon regime were found to shape the early diversification of the genus as well as subsequent radiations during the late Miocene and Pliocene.ConclusionsWe report new evidence for a coincidence of plant diversification and changes of the climate caused by the uplift of the Himalaya. These results are discussed in the context of the impact of incomplete taxon sampling, uncertainty of divergence time estimates, and limitations of current methods used to assess diversification rates.

Phylogeny of the paleotropical fern genus Lepisorus (Polypodiaceae, Polypodiopsida) inferred from four chloroplast DNA regions

Phylogenetic relationships within the paleotropical genus Lepisorus (Polypodiaceae) were investigated using plastid DNA sequences from four regions: rbcL, rps4 and rps4-trnS IGS, trnL intron plus trnL-F IGS, rbcL-atpB IGS. Over 4000 nucleotides were sequenced for 77 specimens belonging to 54 species. Each cpDNA region was analyzed separately and combined into a single dataset. All phylogenetic analyses, maximum parsimony, maximum likelihood and Bayesian Inference of phylogeny, revealed the paraphyly of Lepisorus with the monotypic Drymotaenium miyoshianum and of the paleotropical genus Belvisia nested within the Lepisorus clade. Nine well-supported major clades were found. The phylogenetic results provided new evidence for the sectional classification of Lepisorus. The evolution of three morphological characters, clathrateness of rhizome scales, margin of rhizome scales and defoliated leaves, and the evolution of the karyotype, were reconstructed to identify lineage specific phenotypic character states or combination of characters. Unique character combinations, rather than synapomorphies, were found to be of systematic value in sectional delimitation. The variation of chromosome numbers is largely due to a single aneuploidy event instead of a stepwise reduction during the evolutionary history of this genus.

The microsoroid ferns: Inferring the relationships of a highly diverse lineage of Paleotropical epiphytic ferns (Polypodiaceae, Polypodiopsida)

The relationships of the microsoroid ferns were studied using a DNA sequence-based phylogenetic approach. Nucleotide sequences for up to four chloroplast genome regions were assembled for 107 samples from 87 species. Microsoroids s.l. include six lineages of which two are species rich. The results indicate that several genera are not monophyletic (e.g. Microsorum), several controversial genera are confirmed to be monophyletic (e.g. Leptochilus), and some genera new to science should be recognized (M. membranaceum clade). Unique insights were gained into the biogeographic history of this highly diverse epiphytic vascular plant lineage that is widespread in continental Asia to Australasia. Evidence was found for splits into lineages diversifying in parallel in continental Asia and Malesia. No evidence was recovered for an African radiation because all African microsoroid species either also are found in Asia or have sister species in continental Asia. In contrast, evidence for independent radiations were discovered for the Australasian region.

Exploring generic delimitation within the fern family Thelypteridaceae

Thelypteridaceae is one of the largest families of polypodioid ferns. The generic classification of the family is still controversial because of high levels of convergent or parallel evolution of morphological characters and a lack of molecular phylogenetic studies. In the present study, phylogenetic analyses of three chloroplast regions (rbcL, rps4 and trnL-trnF intergenic spacer region) for 115 taxa, representing 27 recognized segregates in the family, were conducted to explore infrafamilial relationships and gain further understanding of generic boundaries. The phylogenetic reconstructions resolved six distinct clades (Clade I-VI) with strong support. Seven genera: Cyclogramma, Macrothelypteris, Oreopteris, Phegopteris, Pseudophegopteris, Stegnogramma, and Thelypteris are recognized from Clades I, II, IV, and V. In Clade III, Metathelypteris was supported as monophyletic, but the other segregates Amauropelta, Coryphopteris, and Parathelypteris were polyphyletic or paraphyletic, preventing clear recognition of generic boundaries within this clade without additional sampling. Considering great morphological homoplasy within Clade VI, a large genus Cyclosorus is recognized to comprise several small recognized segregates. Within this clade, Pronephrium, and Christella were revealed to be polyphyletic, but several Asian-endemic segregates, such as Glaphyropteridopsis, Mesopteris, and Pseudocyclosorus were strongly supported as monophyletic. Analyses of the evolution of morphological character states on the molecular phylogeny showed extremely high levels of homoplastic evolution for many diagnostic characters.

Indehiscent sporangia enable the accumulation of local fern diversity at the Qinghai-Tibetan Plateau.

BackgroundIndehiscent sporangia are reported for only a few of derived leptosporangiate ferns. Their evolution has been likely caused by conditions in which promotion of self-fertilization is an evolutionary advantageous strategy such as the colonization of isolated regions and responds to stressful habitat conditions. The Lepisorus clathratus complex provides the opportunity to test this hypothesis because these derived ferns include specimens with regular dehiscent and irregular indehiscent sporangia. The latter occurs preferably in well-defined regions in the Himalaya. Previous studies have shown evidence for multiple origins of indehiscent sporangia and the persistence of populations with indehiscent sporangia at extreme altitudinal ranges of the Qinghai-Tibetan Plateau (QTP).ResultsIndependent phylogenetic relationships reconstructed using DNA sequences of the uniparentally inherited chloroplast genome and two low-copy nuclear genes confirmed the hypothesis of multiple origins of indehiscent sporangia and the restriction of particular haplotypes to indehiscent sporangia populations in the Lhasa and Nyingchi regions of the QTP. In contrast, the Hengduan Mountains were characterized by high haplotype diversity and the occurrence of accessions with and without indehiscent sporangia. Evidence was found for polyploidy and reticulate evolution in this complex. The putative case of chloroplast capture in the Nyingchi populations provided further evidence for the promotion of isolated but persistent populations by indehiscent sporangia.ConclusionsThe presented results confirmed the hypothesis that indehiscent sporangia promote the establishment of persistent population in different regions of the QTP. These results are consistent with the expectations of reproductive reassurance by promotion of self-fertilization that played a critical role in the assembly of populations in isolated locations and/or extreme habitats.

Toward a new circumscription of the twinsorus-fern genus Diplazium (Athyriaceae): A molecular phylogeny with morphological implications and infrageneric taxonomy

Diplazium and allied segregates (Allantodia, Callipteris, Monomelangium) represent highly diverse genera belong- ing to the lady-fern family Athyriaceae. Because of the morphological diversity and lack of molecular phylogenetic analyses of this group of ferns, generic circumscription and infrageneric relationships within it are poorly understood. In the present study, the phylogenetic relationships of these genera were investigated using a comprehensive taxonomic sampling including 89 species representing all formerly accepted segregates. For each species, we sampled over 6000 DNA nucleotides of up to seven plastid genomic regions: atpA, atpB, matK, rbcL, rps4, rps4-trnS IGS, and trnL intron plus trnL-trnF IGS. Phylogenetic analyses including maximum parsimony, maximum likelihood and Bayesian methods congruently resolved Allantodia, Cal - lipteris and Monomelangium nested within Diplazium; therefore a large genus concept of Diplazium is accepted to keep this group of ferns monophyletic and to avoid paraphyletic or polyphyletic taxa. Four well-supported clades and eight robust sub- clades were found in the phylogenetic topology. Reconstruction of the evolutionary pattern of morphological characters, such as dissections of leaves, petiole/rachis scales, and shapes of sori, recovered some character combinations of systematic value for infrageneric classification. In light of morphological characters and our molecular phylogeny, a re-defined Diplazium and an infrageneric classification are proposed.

Molecular phylogeny of the endemic fern genera Cyrtomidictyum and Cyrtogonellum (Dryopteridaceae) from East Asia

Cyrtomidictyum Ching and Cyrtogonellum Ching are two eastern Asian endemic genera whose taxonomic affinities and phylogenetic relationships have long been controversial. The main uncertainty surrounds the separation of the two genera from the species-rich genus Polystichum. Here we present a phylogenetic study focusing on the phylogenetic relationships of these polystichoid ferns. We reconstructed the relationships based on DNA sequence variation in four chloroplast genome regions, rbcL, atpB, and the intergenic spacers (IGS) rps4-trnS and trnL-trnF. Maximum likelihood and Bayesian inference analyses confirm earlier results that were based on less comprehensive taxon sampling and either only a single gene (rbcL) or two IGS (rps4-trnS and trnL-trnF). Cyrtomidictyum is the sister of the clade of polystichoid ferns that includes Cyrtogonellum, Cyrtomium subser. Balansana and three sections of Polystichum. Cyrtogonellum groups with several species of Polystichum, and constitutes the sister taxon to Polystichum sect. Sphaenopolystichum. We support the recognition of Cyrtomidictyum as circumscribed initially, rather than expansion of the genus to include either several Polystichum species or Cyrtogonellum, some Polystichum and Cyrtomium species. The monophyly of Cyrtomidictyum is supported by morphological characters such as once-pinnate leaves, free venation, prolongated leaf apices, and exindusiate sori. Two synapomorphic indels in the chloroplast genome, one 15-bp deletion in rps4-trnS, and one 3-bp insertion in trnL-trnF further differentiate Cyrtomidictyum from other polystichoid ferns. The close affinity of Cyrtogonellum to section Sphaenopolystichum of Polystichum s.s. is highly supported by molecular data. However, no shared morphological characters or molecular indels have been detected, although the distinctness of Cyrtogonellum is shown by a 13-bp insertion in the rps4-trnS alignment.

Phylogenetic placement of the enigmatic fern genus Trichoneuron informs on the infra-familial relationship of Dryopteridaceae

The taxonomic status and phylogenetic placement of the monotypic genus Trichoneuron is studied using DNA sequences of three plastid-coding genes. Trichoneuron was originally assigned to Thelypteridaceae but has been considered to be a synonym of Lastreopsis in recent treatments. In this study, the proposed relationship of Trichoneuron to Lastreopsis was tested using a comprehensive taxa sampling of Dryopteridaceae. Our results strongly support the recognition of Trichoneuron as a distinct genus belonging to Dryopteridaceae. Trichoneuron does not group together with Lastreopsis. Instead the genus was found to be sister to the Neotropical genus Polystichopsis. This sister relationship is supported by the occurrence of long pluricellular hairs attached to the rachis of both genera. The morphological distinction of Trichoneuron from Lastreopsis is backed by the structure of the adaxial groove of rachis-costa junction and the hairs at abaxial side of leaf axes. The Polystichopsis–Trichoneuron clade was found to form the sister clade to an entirely Neotropical clade comprising Polybotrya and its relatives. The new subfamily Polybotryoideae is introduced based on the presented observations. In turn, the newly recovered sister relationship between Polystichopsis and Trichoneuron provides evidence for geographic disjunctions involving the Caribbean islands and the Indo–Burma biodiversity hotspot.