Eric Schuettpelz

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.

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.

Accelerated Rate of Molecular Evolution for Vittarioid Ferns is Strong and Not Driven by Selection

Molecular evolutionary rate heterogeneity-the violation of a molecular clock-is a prominent feature of many phylogenetic data sets. It has particular importance to systematists not only because of its biological implications, but also for its practical effects on our ability to infer and date evolutionary events. Here we show, using both maximum likelihood and Bayesian approaches, that a remarkably strong increase in substitution rate in the vittarioid ferns is consistent across the nuclear and plastid genomes. Contrary to some expectations, this rate increase is not due to selective forces acting at the protein level on our focal loci. The vittarioids bear no signature of the change in the relative strengths of selection and drift that one would expect if the rate increase was caused by altered post-mutation fixation rates. Instead, the substitution rate increase appears to stem from an elevated supply of mutations, perhaps limited to the vittarioid ancestral branch. This generalized rate increase is accompanied by extensive fine-scale heterogeneity in rates across loci, genomes, and taxa. Our analyses demonstrate the effectiveness and flexibility of trait-free investigations of rate heterogeneity within a model-selection framework, emphasize the importance of explicit tests for signatures of selection prior to invoking selection-related or demography-based explanations for patterns of rate variation, and illustrate some unexpected nuances in the behavior of relaxed clock methods for modeling rate heterogeneity, with implications for our ability to confidently date divergence events. In addition, our data provide strong support for the monophyly of Adiantum, and for the position of Calciphilopteris in the cheilanthoid ferns, two relationships for which convincing support was previously lacking.

DIVERGENCE TIMES AND THE EVOLUTION OF EPIPHYTISM IN FILMY FERNS (HYMENOPHYLLACEAE) REVISITED

Although the phylogeny of the filmy fern family (Hymenophyllaceae) is rapidly coming into focus, much remains to be uncovered concerning the evolutionary history of this clade. In this study, we use two data sets (108‐taxon rbcL + rps4, 204‐taxon rbcL) and fossil constraints to examine the diversification of filmy ferns and the evolution of their ecology within a temporal context. Our penalized likelihood analyses (with both data sets) indicate that the initial divergences within the Hymenophyllaceae (resulting in extant lineages) and those within one of the two major clades (trichomanoids) occurred in the early to middle Mesozoic. There was a considerable delay in the crown group diversification of the other major clade (hymenophylloids), which began to diversify only in the Cretaceous. Maximum likelihood and Bayesian character state reconstructions across the broadly sampled single‐gene (rbcL) phylogeny do not allow us to unequivocally infer the ancestral habit for the family or for its two major clades. However, adding a second gene (rps4) with a more restricted taxon sampling results in a hypothesis in which filmy ferns were ancestrally terrestrial, with epiphytism having evolved several times independently during the Cretaceous.

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.

Tryonia, a new taenitidoid fern genus segregated from Jamesonia and Eriosorus (Pteridaceae)

Abstract The Neotropical fern genera Eriosorus and Jamesonia have long been thought of as close relatives. Molecular phylogenetic studies have confirmed this notion but have also revealed that neither genus is monophyletic with respect to the other. As a result, all known species of Eriosorus were recently subsumed under the older generic name Jamesonia. Here, through an analysis of a four-gene plastid dataset, we show that several species traditionally treated in Eriosorus are in fact more closely related to other taenitidoid fern genera (namely Austrogramme, Pterozonium, Syngramma, and Taenitis) than they are to the large Jamesonia sensu lato clade. Tryonia Schuettp., J.Prado & A.T.Cochran gen. nov. is described to accommodate these species and four new combinations are provided. Tryonia is confined to southeastern Brazil and adjacent Uruguay; it is distinct (from most species of Jamesonia) in having stramineous rachises.

Maidenhair Ferns, Adiantum, are Indeed Monophyletic and Sister to Shoestring Ferns, Vittarioids (Pteridaceae)

Abstract Across the tree of life, molecular phylogenetic studies often reveal surprising relationships between taxa with radically different morphologies that have long obscured their close affiliations. A spectacular botanical example is Rafflesia, a holoparasite that produces the largest flowers in the world, but that evolved from tiny-flowered ancestors within the Euphorbiaceae. Outside of parasitic lineages, such abrupt transformations are rarely seen. One exception involves the “maidenhair ferns” (Adiantum), which are quintessential ferns: beautifully dissected, terrestrial, and shade loving. The closely related “shoestring ferns” (vittarioids), in contrast, have an extremely simplified morphology, are canopy-dwelling epiphytes, and exhibit greatly accelerated rates of molecular evolution. While Adiantum and the vittarioids together have been shown to form a robust monophyletic group (adiantoids), there remain unanswered questions regarding the monophyly of Adiantum and the evolutionary history of the vittarioids. Here we review recent phylogenetic evidence suggesting support for the monophyly of Adiantum, and analyze new plastid data to confirm this result. We find that Adiantum is monophyletic and sister to the vittarioids. With this robust phylogenetic framework established for the broadest relationships in the adiantoid clade, we can now focus on understanding the evolutionary processes associated with the extreme morphological, ecological, and genetic transitions that took place within this lineage.

A revised generic classification of vittarioid ferns (Pteridaceae) based on molecular, micromorphological, and geographic data

In ferns, as in most branches of the tree of life, phylogenetic analyses of molecular data have greatly improved our ability to identify natural groupings that are subsequently reflected in classifications grounded in the principle of monophyly (Smith & al., 2006; Rothfels & al., 2012; Christenhusz & Chase, 2014). In some cases, the results of such analyses are consistent with earlier notions of relationships inferred from morphological features (Schneider & al., 2009). However, in many other instances, lineages are revealed that are morphologically confounding and we struggle to identify synapomorphies (Sundue & Rothfels, 2014). The pursuit of such defining characteristics is especially problematic when working within a group possessing very limited morphological disparity. The well-defined vittarioid fern clade consists of 100–130 (Lindsay, 2003) highly simplified and predominantly epiphytic species (Fig. 1). These plants, characterized by the presence of silica bodies (Sundue, 2009) but a lack of sclerenchyma (Bower 1928; Ruhfel & al., 2008), were long regarded as composing a distinct family—Vittariaceae (Ching, 1940; Tryon & Tryon, 1982; Kramer, 1990). However, phylogenetic analyses have demonstrated that these ferns nest well within the Pteridaceae (Crane & al., 1995; Hasebe & al., 1995; Prado & al., 2007; Schuettpelz & al., 2007), as sister to the genus Adiantum L. (Lu & al., 2012; Rothfels & Schuettpelz, 2014; Pryer & al., 2016). The vittarioids have been variously partitioned through time (Benedict, 1911; Williams, 1927; Copeland, 1947). In the years leading up to the first molecular phylogenetic analyses of these ferns, six genera were commonly recognized based primarily on leaf division, venation, and the distribution of A revised generic classification of vittarioid ferns (Pteridaceae) based on molecular, micromorphological, and geographic data

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.