Toward a monophyletic Notholaena (Pteridaceae): resolving patterns of evolutionary convergence in xeric-adapted ferns

With over 1,000 species, Pteridaceae comprises approximately 10% of extant fern diversity and is notable for its extreme morphological and ecological disparity. In addition to species-rich and predominantly forest-dwelling genera such as Adiantum and Pteris, the family includes floating, freshwater aquatics (Ceratopteris), mangrove specialists (Acrostichum), obligate epiphytes (Vittaria), and epipetric xerophytes (Cheilanthes, Notholaena, Pellaea). The ability of some species of Pteridaceae to flourish in arid environments (Yatskievych & Hooper, 2001) is particularly striking given that moisture dependence is often considered an ecologically limiting factor for ferns (Page, 2002). Pteridaceae includes both facultative and obligate xerophytes, nearly all of which are members of the well-supported cheilanthoid clade (sensu Schuettpelz & al., 2007), which contains an estimated 400 species. Cheilanthoids exhibit extensive disparity in both their gross morphology (leaf shape) and their reproductive structures (particularly sporangial arrangement and type of indusium). For example, Hemionitis palmata has undivided palmate leaves with unprotected sporangia spread along the veins (Fig. 1A); Pellaea intermedia has bipinnate leaves and sporangia near vein tips where they are protected by an inrolled leaf margin (false indusium, Fig. 1B); Astrolepis sinuata has linear leaves, with sporangia densely covered with scales (Fig. 1C); Notholaena rosei has linear-lanceolate leaves and submarginal sporangia nestled among dense flavonoid deposits (“farina”, Fig. 1D); and Adiantopsis radiata has palmately compound leaf architecture, and sporangia protected by discrete, flap-like false indusia (Fig. 1E). Counterintuitively, these highly divergent morphologies do not correspond with monophyletic genera. Cheilanthoids, rather, have been called “the most contentious group of ferns with respect to a practical and natural generic classification” (Tryon & Tryon, 1982). This historic inability to identify monophyletic genera among cheilanthoid ferns is frequently attributed to convergent evolution (morphological homoplasy) driven by their adaptation to arid habitats (Tryon & Tryon, 1973; Lellinger, 1989; Gastony & Rollo, 1998; Kirkpatrick, 2007; Prado & al., 2007). Generic circumscriptions among cheilanthoid ferns are thus notoriously unstable, varying radically by author and geographic region. One of the best examples of this taxonomic confusion involves the genus Notholaena R. Br. Circumscriptions of this genus range from narrow (including only those species with farinose sporophytes and gametophytes, e.g., Windham, 1993a) to very broad (including taxa as disparate as Argyrochosma, Astrolepis, Toward a monophyletic Notholaena (Pteridaceae): resolving patterns of evolutionary convergence in xeric-adapted ferns