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Evolution and Phylogeny of Gnetophytes: Evidence from the Anatomically Preserved Seed Cone Protoephedrites Eamesii Gen

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Evolution and Phylogeny of Gnetophytes: Evidence from the Anatomically Preserved Seed Cone Protoephedrites Eamesii Gen Evolution and Phylogeny of Gnetophytes: Evidence from the Anatomically Preserved Seed Cone Protoephedrites eamesii gen. et sp. nov. and the Seeds of Several Bennettitalean Species Author(s): Gar W. Rothwell and Ruth A. Stockey Source: International Journal of Plant Sciences, Vol. 174, No. 3, Special Issue: Conceptual Advances in Fossil Plant Biology Edited by Gar Rothwell and Ruth Stockey (March/April 2013), pp. 511-529 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/668688 . Accessed: 22/04/2013 15:53 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to International Journal of Plant Sciences. http://www.jstor.org This content downloaded from 128.193.162.72 on Mon, 22 Apr 2013 15:53:03 PM All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 174(3):511–529. 2013. Ó 2013 by The University of Chicago. All rights reserved. 1058-5893/2013/17403-0020$15.00 DOI: 10.1086/668688 EVOLUTION AND PHYLOGENY OF GNETOPHYTES: EVIDENCE FROM THE ANATOMICALLY PRESERVED SEED CONE PROTOEPHEDRITES EAMESII GEN. ET SP. NOV. AND THE SEEDS OF SEVERAL BENNETTITALEAN SPECIES Gar W. Rothwell1,*,y and Ruth A. Stockeyy,z *Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, U.S.A.; yDepartment of Botany and Plant Pathology, 2082 Cordley Hall, Oregon State University, Corvallis, Oregon 97331, U.S.A.; and zDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada A fossil seed cone with characters that have been hypothesized as transitional to the origin of crown group gnetophytes has been discovered in Lower Cretaceous deposits on Vancouver Island, British Columbia, Canada. This cone, described as Protoephedrites eamesii gen. et sp. nov., provides the first anatomically preserved fossil evidence for the evolution of gnetophyte cones with seeds. The cone is a compound shoot system consisting of a primary axis with nodes that bear bracts and axillary fertile shoots in an opposite/ decussate arrangement. The secondary fertile shoot axis produces one or two pairs of diminutive bracteoles and a pair of erect ovules in an opposite/decussate pattern. In contrast to crown group gnetophytes, bracteoles subtend rather than surround and enclose the ovules. Ovules have a single multiseriate integument that is adnate to the nucellus in the basal region and free distally. The micropylar tube is short with a thick integument, but it displays distinctive cells of the inner integumentary epidermis that are characteristic of gnetophyte seeds. Each seed produces a large pollen chamber with a uniseriate wall. Paired erect ovules conform to the pleisomorphic morphology previously hypothesized for Ephedra seed cones, thus supporting the proposal that ancestral gnetophyte seeds are borne terminally on oppositely arranged sporophylls. The combination of gnetophyte synapomorphies and putative pleisomorphic characters displayed by Protoephedrites broadens the known range of morphologies for the most ancient gnetophytes. Detailed comparisons to several species of Bennettitales confirm that there are fundamental structural differences separating the seeds of Gnetales from those of Bennettitales, support the hypothesis that the outer seed envelope evolved within the gnetophyte clade, and suggest that Bennettitales are not as closely related to Gnetales as hypothesized by some authors. Keywords: Bennettitales seeds, Cretaceous, evolution, fossil Gnetales, seed cone anatomy, seed plant phylogeny. Online enhancement: video. Introduction characters usually resolve gnetophytes as the sister group to flowering plants at the apex of the spermatophyte tree Gnetophytes are among the most systematically important (Laconte and Stevenson 1990; Doyle and Donoghue 1992; and persistently discussed clades of living seed plants, being Nixon et al. 1994; Rothwell and Serbet 1994; Doyle 1998; repeatedly implicated in both the phylogeny of conifers and Hilton and Bateman 2006; Friis et al. 2007; Rothwell et al. in the origin of flowering plants (Doyle 1998; Mathews 2009), the results of analyses based on nucleotide sequence 2009). Yet, they are also one of the most enigmatic clades of characters of living species yield several conflicting topologies spermatophytes (Burleigh and Mathews 2004, 2007a, 2007b; (Rydin et al. 2002; Mathews 2009). Results of analyses Friis et al. 2007; Rothwell et al. 2009). Because of a unique based on some nucleotide sequences and employing certain suite of distinctive morphological characters (Chamberlain model assumptions resolve gnetophytes at the basal branch 1935; Eames 1952; Rydin et al. 2006a, 2006b; Friis et al. of the extant spermatophyte tree, while analyses of other nu- 2011) and long-branch separation from other spermato- cleotide sequences and/or employing other model assump- phytes in many nucleotide sequence phylogenies (Graham tions resolve gnetophytes either as the sister group to conifers and Isles 2009), systematic relationships and evolutionary or- or as variously nested within the conifer clade (Rydin et al. igins of the clade remain obscure (Mathews 2009; Taylor 2002; Rai et el. 2003, 2008; Mathews 2009; Finet et al. et al. 2009). Whereas systematic analyses of morphological 2010; Rai and Graham 2010). The paleontological record of gnetophytes also remains 1 Author for correspondence; e-mail: [email protected]. equivocal with respect to the most ancient occurrence, ances- Manuscript received April 2012; revised manuscript received October 2012. tral morphological characters, systematic relationships, and 511 This content downloaded from 128.193.162.72 on Mon, 22 Apr 2013 15:53:03 PM All use subject to JSTOR Terms and Conditions 512 INTERNATIONAL JOURNAL OF PLANT SCIENCES phylogeny of the clade (Crane 1996; Rothwell et al. 2009; Tay- In this study, we describe the first permineralized fossil lor et al. 2009). On the basis of primarily palynological records evidence for reproductive anatomy and morphology of (Mu¨ller 1984; Osborn et al. 1993) or pollen contained within gnetophyte cones from the Valanginian Stage of the Lower compressed fructifications that lack the structural synapomor- Cretaceous, ;136 Ma. Protoephedrites eamesii gen. et sp. phies of gnetophytes (Taylor et al. 2009), some authors suspect nov. conforms to the morphology of a hypothesized struc- that the clade originated as early as the Permian (Wang 2004). tural intermediate in a previously proposed transformational There are intriguing gnetophyte-like megafossils in deposits as series leading to the basal crown group gnetophyte genus old as the Triassic (Ash 1972). However, specimens that display Ephedra (Thoday and Berridge 1912; Eames 1952; Ickert- a wide array of widely accepted synapomorphies for gneto- Bond et al. 2009), thus documenting a putative ancestral phytes appear first in the Lower Cretaceous (Crane and morphology and anatomy of gnetophyte seed cones and con- Upchurch 1987; Martill et al. 1993; Taylor et al. 2009; Friis firming hypothesized homologies of the seed position and et al. 2011; Kunzmann et al. 2011) at about the same time as ‘‘outer integumentary envelope’’ that characterize crown the oldest unequivocal megafossil evidence for flowering plants group gnetophytes. The new genus provides additional evi- (Yang et al. 2005; Friis et al. 2011). dence that the outer envelope of gnetophyte seeds evolved Palynological and dispersed seed data reveal that gnetophytes within the gnetophyte clade and that the outer integument diversified along with the flowering plants in the Lower Creta- of gnetophyte and angiosperm seeds evolved by parallel ceous (Crane and Lidgard 1989, 1990; Dilcher et al. 2005; evolution. Friis et al. 2011, 2013) but apparently suffered declining diver- Description of this new cone also provides an opportunity sity later in the Cretaceous (Crane and Lidgard 1990) and Pa- to refigure and analyze the seeds of several bennettitalean leogene (Taylor et al. 2009). The vast majority of Cretaceous species to the seeds of gnetophytes for a critical comparison gnetophyte megafossils are preserved as compression/impressions to the ovulate structures of Gnetales. This comparison em- (Mohr et al. 2007; for a review, see Friis et al. 2011), many phasizes that the seeds and seed-bearing structures of Gne- of which are similar to crown group species of Ephedra tales and Bennettitales show far fewer similarities than L., Welwitschia Hooker, and Gnetum L. (Dilcher et al. 2005; differences and are clearly much more structurally divergent Taylor et al. 2009; Friis et al. 2011), but those fossils provide than recently has been hypothesized by other authors (Friis little evidence for the structural transformations that led to et al. 2007, 2009, 2011, 2013). As a result, it becomes clear the origin and early diversification of the gnetophyte clade. that ovulate reproductive structures of gnetophytes share Heretofore, the almost total absence of permineralized fossil more morphological characters with Paleozoic cordaites and
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