Xin-Mao Zhou

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 large‐scale phylogeny of the lycophyte genus Selaginella (Selaginellaceae: Lycopodiopsida) based on plastid and nuclear loci

The lycophyte genus Selaginella alone constitutes the family Selaginellaceae, the largest of the lycophyte families. The genus is estimated to contain 700–800 species distributed on all continents except Antarctica, with highest species diversity in tropical and subtropical regions. The monophyly of Selaginella in this broad sense has rarely been doubted, whereas its intrageneric classification has been notoriously contentious. Previous molecular studies were based on very sparse sampling of Selaginella (up to 62 species) and often used DNA sequence data from one genome. In the present study, DNA sequences of one plastid (rbcL) and one nuclear (ITS) locus from 394 accessions representing approximately 200 species of Selaginella worldwide were used to infer a phylogeny using maximum likelihood, Bayesian inference and maximum parsimony methods. The study identifies strongly supported major clades and well resolves relationships among them. Major results include: (i) six deep‐level clades are discovered representing the deep splits of Selaginella; and (ii) 20 major clades representing 20 major evolutionary lineages are identified, which differ from one another in molecular, macro‐morphological, ecological and spore features, and/or geographical distribution.

A global plastid phylogeny of the brake fern genus Pteris (Pteridaceae) and related genera in the Pteridoideae

The brake fern genus Pteris belongs to the Pteridaceae subfamily Pteridoideae. It contains 200–250 species distributed on all continents except Antarctica, with its highest species diversity in tropical and subtropical regions. The monophyly of Pteris has long been in question because of its great morphological diversity and because of the controversial relationships of the Australian endemic monospecific genus Platyzoma. The circumscription of the Pteridoideae has likewise been uncertain. Previous studies typically had sparse sampling of Pteris species and related genera and used limited DNA sequence data. In the present study, DNA sequences of six plastid loci of 146 accessions representing 119 species of Pteris (including the type of the genus) and 18 related genera were used to infer a phylogeny using maximum‐likelihood, Bayesian‐inference and maximum‐parsimony methods. Our major results include: (i) the previous uncertain relationships of Platyzoma were due to long‐branch attraction; (ii) Afropteris, Neurocallis, Ochropteris and Platyzoma are all embedded within a well‐supported Pteris sensu lato; (iii) the traditionally circumscribed Jamesonia is paraphyletic in relation to a monophyletic Eriosorus; (iv) Pteridoideae contains 15 genera: Actiniopteris, Anogramma, Austrogramme, Cerosora, Cosentinia, Eriosorus, Jamesonia, Nephopteris (no molecular data), Onychium, Pityrogramma, Pteris, Pterozonium, Syngramma, Taenitis and Tryonia; and (v) 15 well‐supported clades within Pteris are identified, which differ from one another on molecular, morphological and geographical grounds, and represent 15 major evolutionary lineages.

Circumscription and phylogeny of the fern family Tectariaceae based on plastid and nuclear markers, with the description of two new genera: Draconopteris and Malaifilix (Tectariaceae)

The circumscription and the phylogeny of the fern family Tectariaceae have been controversial. Previous molecular studies have supported the monophyly of this family, with 4-5 genera. However, these studies were exclusively based on plastid markers and relatively small sampling, especially of the non-Tectaria genera. In the present study, DNA sequences of eight plastid and one nuclear markers of 25 accessions representing 19 species of Tectaria and 58 accessions representing ca. 90% of the non-Tectaria species in the family (including Arthropteris) were used to infer a phylogeny using maximum likelihood (ML), Bayesian inference, and maximum parsimony. Our major results include: (1) Tectaria as currently circumscribed is not monophyletic and can be divided into three genera: Tectaria s.str., Draconopteris (gen. nov.) from Central to South America, and Malaifilix (gen. nov.) from Malesia; (2) Draconopteris and Malaifilix, the two new genera, together with Pteridrys, form a strongly supported Glade; (3) in our ML analyses, the Glade containing Draconopteris, Malaifilix, and Pteridrys (the DMP Glade) is resolved as sister to the rest of Tectariaceae and Arthropteris is sister to Tectaria+(Hypoderris + Triplophyllum), suggesting that Arthropteris should be treated as a member of Tectariaceae, and thus Tectariaceae contains seven genera: Arthropteris, Draconopteris, Hypoderris, Malaifilix, Pteridrys, Tectaria, and Triplophyllum; (4) with the well-supported relationships among the members of Tectariaceae, anastomosing venation in the family is inferred to have evolved independently at least three times; (5) Nephrolepis is strongly supported as sister to a Glade containing Cyclopeltis, Dracoglossum, and Lomariopsis, and thus we advocate that Lomariopsidaceae include these four genera (plus the unsampled Thysanosoria); and (6) intercontinental dispersal appears to have played an important role in shaping the extant distribution of Tectariaceae.

A well-sampled phylogenetic analysis of the polystichoid ferns (Dryopteridaceae) suggests a complex biogeographical history involving both boreotropical migrations and recent transoceanic dispersals.

Intercontinental disjunctions in ferns have often been considered as the result of long-distance dispersal (LDD) events rather than of vicariance. However, in many leptosporangiate groups, both processes appear to have played a major role in shaping current geographical distribution. In this study, we reconstructed the phylogenetic relationships and inferred the ancestral distribution areas of the polystichoid ferns (Cyrtomium, Phanerophlebia, and Polystichum), to evaluate the relative impact of vicariance and LDD on the biogeography of this group. We used a molecular dataset including 3346 characters from five plastid loci. With 190 accessions our taxon coverage was about three times as large as any previous worldwide sampling. Biogeographical analyses were performed using S-DIVA and S-DEC and divergence times were estimated by integrating fossil and secondary calibrations. The polystichoid ferns are a monophyletic clade that may have originated in East Asia during the Eocene, an age much younger than previously estimated. Three transoceanic disjunctions between East Asia and New World were identified in the Paleogene: one for Phanerophlebia during late Eocene (34Ma, 19-51Ma), and two in Polystichum at the Eocene-Oligocene boundary (30Ma, 18-43Ma; 28Ma, 19-39Ma respectively). During the Neogene, further range expansions took place from Asia to Africa, Hawaii, and the Southwestern Indian Ocean region. Our results indicate that early transfers between the Old and the New World are compatible with a boreotropical migration scenario. After evolving in Asia during the Eocene, the polystichoid ferns reached the New World in independent migrations at the Eocene-Oligocene boundary through the boreotropical belt. However, although less likely, the alternative hypothesis of independent transoceanic dispersals from the Old to the New World cannot be ruled out. Further range expansion during the Neogene was most likely the result of long-distance dispersal (LDD).

Using a multilocus phylogeny to test morphology-based classifications of Polystichum (Dryopteridaceae), one of the largest fern genera

BackgroundPolystichum (Dryopteridaceae) is probably the third largest fern genus in the world and contains ca. 500 species. Species of Polystichum occur on all continents except Antarctica, but its highest diversity is found in East Asia, especially Southwest China and adjacent regions. Previous studies typically had sparse taxon sampling and used limited DNA sequence data. Consequently, the majority of morphological hypotheses/classifications have never been tested using molecular data.ResultsIn this study, DNA sequences of five plastid loci of 177 accessions representing ca. 140 species of Polystichum and 13 species of the closely related genera were used to infer a phylogeny using maximum likelihood, Bayesian inference, and maximum parsimony. Our analyses show that (1) Polystichum is monophyletic, this being supported by not only molecular data but also morphological features and distribution information; (2) Polystichum is resolved into two strongly supported monophyletic clades, corresponding to the two subgenera, P. subg. Polystichum and P. subg. Haplopolystichum; (3) Accessions of P. subg. Polystichum are resolved into three major clades: clade K (P. sect. Xiphophyllum), clade L (P. sect. Polystichum), and the HYMASO superclade dominated by accessions of P. sect. Hypopeltis, P. sect. Macropolystichum, and P. sect. Sorolepidium, while those of P. subg. Haplopolystichum are resolved into eight major clades; and (4) The monophyly of the Afra clade (weakly supported), the Australasian clade (weakly supported), and the North American clade (strongly supported) is confirmed.ConclusionsOf the 23 sections of Polystichum recognized in a recent classification of the genus, four (P. sect. Hypopeltis, P. sect. Neopolystichum, P. sect. Sorolepidium, P. sect. Sphaenopolystichum) are resolved as non-monophyletic, 16 are recovered as monophyletic, and three are monospecific. Of the 16 monophyletic sections, two (P. sect. Adenolepia, P. sect. Cyrtogonellum) are weakly supported and 14 are strongly supported as monophyletic. The relationships of 11 sections (five in P. subg. Haplopolystichum; six in P. subg. Polystichum) are well resolved.

A global phylogeny of the fern genus Tectaria (Tectariaceae: Polypodiales) based on plastid and nuclear markers identifies major evolutionary lineages and suggests repeated evolution of free venation from anastomosing venation

Tectaria (Tectariaceae) is one of the most confusing fern genera in terms of its circumscription and phylogeny. Since its original description, a number of genera had been moved into or related with this genus, while others had been segregated from it. Tectaria is also among the largest fern genera, comprising 150-210 mostly tropical species. Previous molecular studies have been far from comprehensive (sampling no more than 76 accessions from 52 species), limited in geographic scope (mainly restricted to Asia), and based exclusively on plastid markers. In the present study, DNA sequences of eight plastid and one nuclear marker of 360 accessions representing ca. 130 species of Tectaria, ca. 36 species of six non-Tectaria genera in Tectariaceae, 12 species of Davalliaceae, Oleandraceae, and Polypodiaceae, and 13 species of Lomariopsidaceae were used to infer a phylogeny with maximum likelihood, Bayesian inference, and maximum parsimony approaches. Our major results include: (1) the most recently proposed circumscription of Tectaria is strongly supported as monophyletic; (2) the genera Lenda, Microbrochis, Phlebiogonium, and Sagenia, sampled here for the first time, are resolved as part of Tectaria; (3) four superclades representing early splits in Tectaria are identified, with the Old World species being sister to the New World species; (4) 12 well-supported major clades in Tectaria are revealed, differing from one another in molecular, morphological, and geographical features; (5) evolution of 13 morphological characters is inferred in a phylogenetic context and morphological synapomorphies of various clades are identified; and in particular (6) free venation in Tectaria is inferred to be repeatedly derived from anastomosing venation, an evolutionary phenomenon not documented previously in vascular plants in a phylogenetic context based on both plastid and nuclear evidence.

Phylogeny of the fern subfamily Pteridoideae (Pteridaceae; Pteridophyta), with the description of a new genus: Gastoniella

As the second most genera-rich fern family, Pteridaceae contain more than 1000 species contributing to ca. 10% of extant leptosporangiate fern diversity. The subfamily Pteridoideae is one of the five subfamilies often recognized. The circumscription of Pteridoideae has not been clear. A large number of species have not yet been included in any molecular analyses before. In this study, DNA sequences of six plastid loci of 154 accessions representing ca. 87 species in 14 genera of Pteridaceae subfam. Pteridoideae and four accessions representing two species in subfam. Parkerioideae and one species of subfam. Adiantoideae as outgroups were used to infer a phylogeny using maximum likelihood and maximum parsimony. Our analyses show that (1) Pteridoideae is monophyletic and the newly defined subfamily is composed of 14 genera including a newly described genus; (2) Pteridoideae is resolved into four strongly supported monophyletic clades: the Pteris clade, the Actiniopteris+Onychium clade, the JAPSTT clade, and the GAPCC clade, these being supported by not only molecular data but also morphological features and distribution information; (3) Onychium is confirmed as monophyletic and accessions of Onychium are resolved into two strongly supported clades, the O. cryptogrammoides clade and the O. siliculosum clade; and (4) Accessions of the traditionally defined Anogramma are resolved as paraphyletic in relation to Cerosora, Cosentinica, and Pityrogramma. Three species traditionally treated in Anogramma are in fact more closely related to Cerosora and Pityrogramma than they are to Anogramma. Gastoniella Li Bing Zhang & Liang Zhang, gen. nov. is described to accommodate these species and three new combinations are provided. Three currently known species of Gastoniella are distributed in the Ascension Island in South Atlantic Ocean, central Mexico, and tropical America, respectively. The new genus is distinct from Anogramma s.s. in having ultimate segments linear not obviously broadening toward the upper portion.

A plastid phylogeny and character evolution of the Old World fern genus Pyrrosia (Polypodiaceae) with the description of a new genus: Hovenkampia (Polypodiaceae)

The Old World fern genus Pyrrosia (Polypodiaceae) offers a rare system in ferns to study morphological evolution because almost all species of this genus are well studied for their morphology, anatomy, and spore features, and various hypotheses have been proposed in terms of the phylogeny and evolution in this genus. However, the molecular phylogeny of the genus lags behind. The monophyly of the genus has been uncertain and a modern phylogenetic study of the genus based on molecular data has been lacking. In the present study, DNA sequences of five plastid markers of 220 accessions of Polypodiaceae representing two species of Drymoglossum, 14 species of Platycerium, 50 species of Pyrrosia, and the only species of Saxiglossum (subfamily Platycerioideae), and 12 species of other Polypodiaceae representing the remaining four subfamilies are used to infer a phylogeny of the genus. Major results and conclusions of this study include: (1) Pyrrosia as currently circumscribed is paraphyletic in relation to Platycerium and can be divided into two genera: Pyrrosia s.s. and Hovenkampia (gen. nov.), with Hovenkampia and Platycerium forming a strongly supported clade sister to Pyrrosia s.s.; (2) Subfamily Platycerioideae should contain three genera only, Hovenkampia, Platycerium, and Pyrrosia s.s.; (3) Based on the molecular phylogeny, macromorphology, anatomical features, and spore morphology, four major clades in the genus are identified and three of the four are further resolved into four, four, and six subclades, respectively; (4) Three species, P. angustissima, P. foveolata, and P. mannii, not assigned to any groups by Hovenkamp (1986) because of their unusual morphology, each form monospecific clades; (5) Drymoglossum is not monophyletic and those species previously assigned to this genus are resolved in two different subclades; (6) Saxiglossum is resolved as the first lineage in the Niphopsis clade; and (7) The evolution of ten major morphological characters in the subfamily is inferred based on the phylogeny and various morphological synapomorphies for various clades and subclades are identified.

A global plastid phylogeny uncovers extensive cryptic speciation in the fern genus Hymenasplenium (Aspleniaceae)

The fern genus Hymenasplenium (Aspleniaceae) is one of the two genera in the family. It is generally recognized among modern pteridologists. However, its infrageneric relationships and species diversity have been unclear and controversial. The molecular studies so far have had small taxon and character sampling. In the present study, DNA sequences of six plastid markers of 158 accessions representing ca. 40 out of ca. 50 known species of Hymenasplenium, and 16 species of Asplenium were used to infer a phylogeny with maximum likelihood, Bayesian inference, and maximum parsimony approaches. Our major results include: (1) Hymenasplenium as currently defined is strongly supported as monophyletic; (2) three major clades representing early splits in Hymenasplenium are identified, with the Old World species being strongly supported as monophyletic; it is ambiguous if the New World species are monophyletic; (3) extensive cryptic speciation in the Old World is discovered demonstrating the complexity of evolution of the genus; and (4) six strongly or moderately supported subclades in the Old World clade are revealed, differing from one another in molecular, morphological, and geographical features.