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Paleobotany |
2 Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701 USA 3 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
Received for publication 7 August 2007. Accepted for publication 24 January 2008.
ABSTRACT
The first fossil evidence for the fern genus Todea has been recovered from the Lower Cretaceous of British Columbia, Canada, providing paleontological data to strengthen hypotheses regarding patterns of evolution and phylogeny within Osmundaceae. The fossil consists of a branching rhizome, adventitious roots, and leaf bases. The dictyoxylic stem has up to eight xylem bundles around a sclerenchymatous pith. Leaf traces diverge from cauline bundles in a typical osmundaceous pattern and leaf bases display a sheath of sclerenchyma around a C-shaped xylem trace with 2–8 protoxylem strands. Within the adaxial concavity of each leaf trace, a single sclerenchyma bundle becomes C-shaped as it enters the cortex. The sclerotic cortex is heterogeneous with an indistinct outer margin. The discovery of Todea tidwellii sp. nov. reveals that the genus Todea evolved by the Lower Cretaceous. A phylogenetic analysis combining morphological characters of living and extinct species with a previously published nucleotide sequence matrix confirms the taxonomic placement of T. tidwellii. Results also support the hypothesis that Osmunda s.l. represents a paraphyletic assemblage and that living species be segregated into two genera, Osmunda and Osmundastrum. Fossil evidence confirms that Osmundaceae originated in the Southern Hemisphere during the Permian, underwent rapid diversification, and species extended around the world during the Triassic. Crown group Osmundaceae originated by the Late Triassic, with living species appearing by the Late Cretaceous.
Key Words: Cretaceous • fern phylogeny • Osmundaceae • Osmundastrum • rhizome • Todea
Abundant fern fossils representing the family Osmundaceae L. occur in deposits that range from the Upper Permian to the Recent (Miller, 1971
; Tidwell and Ash, 1994), providing a wealth of data for inferring patterns of leptosporangiate fern evolution and phylogeny. The Osmundaceae traditionally has been regarded as the most basal family of living Filicales (Bower, 1926; Wagner, 1969; Bierhorst, 1971; Holttum, 1973), probably diverging from an extinct filicalean sister group in the Upper Pennsylvanian or Lower Permian (Miller, 1971; Tidwell and Ash, 1994). That systematc hypothesis is supported by recent phylogenetic analyses of both morphological and nucleotide sequence characters (Rothwell, 1999; Smith et al., 2006). The genus Osmunda L. s.l. is also extremely ancient, extending from the mid-Triassic (Phipps et al., 1998), with at least one living species (O. cinnamomea L.) having evolved by the Upper Cretaceous (Serbet and Rothwell, 1999). While there are more than 200 species of fossil osmundaceous ferns worldwide (Stewart and Rothwell, 1993; Taylor and Taylor, 1993; Tidwell and Ash, 1994), living representatives of the family are restricted to a small number of genera with a total of only 14–21 species (Kramer, 1990). These traditionally have been understood as conforming to three genera: Osmunda, Leptopteris Presl., and Todea Willdenow ex Bernhardi, with Osmunda being widely recognized as forming three natural groups, Osmunda, Osmundastrum, and Plenasium (Diels, 1898; Clausen, 1938; Hewitson, 1962; Miller, 1967).
Although the paleontological record of Osmundaceae is exceedingly rich, most osmundaceous fossils are assigned to morphotaxa because they consist of either compressed frond fragments or anatomically preserved rhizomes/rachides that cannot be assigned with confidence to genera with living species (Miller, 1971; Tidwell and Ash, 1994). Whole-plant concepts have yet to be developed for extinct genera and species. Nevertheless, there is a growing fossil record for the genus Osmunda, which has provided a wealth of data for inferring evolution and phylogeny of the family (Phipps et al., 1998; Serbet and Rothwell, 1999; Vavrek et al., 2006). Fossil remains for Todea and Leptopteris have not been described previously.
Over the past several years Lower Cretaceous deposits at Apple Bay on Vancouver Island along the west coast of southern British Columbia, Canada have yielded large numbers of plant fossils with superb anatomical preservation (Stockey and Rothwell, 2006). These include fertile frond segments described as Osmunda vancouverensis Vavrek, Stockey et Rothwell and the first fossil evidence for the genus Todea, which is the focus of the current study. The material consists of a permineralized rhizome with attached leaf bases and adventitious roots, and is described as Todea tidwellii sp. nov. Several distinctive characters reveal that T. tidwellii is assignable to the genus Todea, but other features distinguish it from the two living species T. barbara (L.) Moore and T. papuana Hennipman.
A phylogenetic analysis was conducted that combined morphological characters of living and extinct species with data from a previously published nucleotide sequence matrix (Yatabe et al., 1999). Results of that analysis confirm the assignment of T. tidwellii to the genus Todea and resolve Osmunda s.l. as a paraphyletic assemblage. That analysis supports the segregation of living Osmunda species to at least two genera, including Osmundastrum for O. cinnamomea and Osmunda for the remaining species. The results strengthen hypotheses that crown group Osmundaceae evolved before the breakup of Pangaea, explaining the worldwide distribution of living species, and inferring that broad laminar fertile pinnules may be derived within the crown group.
MATERIALS AND METHODS
The current study is based on a fossil rhizome found in the Lower Cretaceous (Hauterivian–Valanginian) sediments on the shore of Apple Bay, Vancouver Island, British Columbia, Canada (49°54'42''N, 125°10'40''; UTM 10U CA 5531083N 343646E; Smith et al., 2003). The rhizome is preserved in a greywacke matrix as an isolated calcareous cellular permineralization. The specimen was exposed in an oblique longitudinal plane on the surfaces of two adjacent blocks. The two surfaces were photographed (e.g., Fig. 1), glued back together with epoxy, cut into wafers 
1 cm thick, and then serially sectioned in both transverse and longitudinal views (Figs. 2–9) by the cellulose acetate peel technique (Joy et al., 1956). Peels for microscopic examination and image capture were mounted on microscope slides with Eukitt mounting medium (O. Kindler GmbH, Freiburg, Germany). Images were captured with Microlumina (Leaf Systems, Bedford, Massachusetts, USA) and Photophase (Phase One A/S, Frederiksberg, Denmark) digital scanning cameras and processed with Adobe Photoshop (San Jose, California, USA). Specimens, peels, and microscope slides are housed at University of Alberta Paleobotanical Collections, Edmonton, Alberta, Canada.
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). Aligned sequence data from an earlier analysis (i.e., 1227 characters; Yatabe et al., 1999) were supplemented by a newly developed matrix of 41 morphological characters (Appendix 1) for six living Osmundaceous species representing each of the subgenera of Osmunda [i.e., O. cinnamomea, O. regalis L, O. vachellii (C. Presl.) Hook], one living species each of Leptopteris and Todea [i.e., L. hymenophyllides (A. Rich.) C. Presl., T. barbara (L.) Moore], and T. tidwellii. As in the earlier analysis by Yatabe et al. (1999) two geographically distant representatives of O. cinnamomea and O. claytonia were included in our analyses, and each species pair resolved as sisters in the results. For clarity of the overall pattern of cladistic relationships, only one terminal of each species pair is included in the figured phylogeny (Fig. 12). The matrix also included Ophioglossum reticulatum L., Angiopteris lygodifolia Ros., Cephalomanes thysanostomum (Makino) K. Iwats., Gleichenia japonica Spr., Lygodium japonicum (Thumb) Sw., Dryopteris cristata (L.) Gray, and Stegnogramma pozoi (Lagasca) K. Iwats. as outgroups. The outgroups have been condensed to a single taxon in the results (Fig. 12). Character concepts and state definitions for morphological characters are presented in Appendix 2.
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) performed in a Dell (Round Rock, Texas, USA) Inspiron 8600 personal computer using the program NONA (Goloboff, 1999), spawned through the program Winclada (Asado, version 1.1 beta, by K. Nixon, Cornell University). To minimize a priori assumptions about the relative value of characters, all characters were unweighted and unpolarized, and multistate characters were unordered. Branch support was estimated by the bootstrap option in Winclada. SYSTEMATICS
Specific diagnosis
Small osmundaceous trunks with closely spaced frond bases and adventitious roots. Rhizomes 4.5 cm long, up to 3 cm wide; branching distally; phyllotaxis helical; with heterogeneous sclerotic cortex. Cortex with indistinct outer boundary and prominent sclerotic ring surrounding frond and root traces from inner margin of sclerotic cortex. Rhizome dictyoxylic and ectophloic, with up to five cauline bundles and thin C-shaped leaf traces; one foliar protoxylem at divergence of trace, dividing in two in inner cortex, and increasing to six to eight in stipe base. Pith sclerenchymatous, up to 2 mm in maximum diameter; sclerenchyma lobes of pith diverge as a rod adaxial to each leaf trace becoming C-shaped at stipe base. Sclerotic ring of stipe heterogeneous; thinner adaxially. Diarch adventitious roots diverging from cauline bundles, one per frond.
Holotype hic designatus
Permineralized slabs, peels, and slides of specimen P14,466 housed in the University of Alberta Paleobotanical Collection (UAPC-ALTA), Edmonton, Alberta.
Collecting locality
Apple Bay, northern Vancouver Island, British Columbia, Canada (50°36'21''N, 127°39'25''W; UTM 9U WG 951068).
Stratigraphic position and age
Longarm Formation equivalent. Valanginian–Hautervian boundary, Early Cretaceous.
Etymology
The specific epithet tidwellii is proposed in honor of William D. (Don) Tidwell, Brigham Young University, for his numerous contributions to our understanding of fossil Osmundaceae.
RESULTS
Todea tidwellii is represented by a small trunk that consists of a branching stem with closely spaced, diverging frond bases and root traces (Fig. 1). The specimen is roughly conical, at least 4.5 cm long, 3.0 cm in maximum width at the distal end, and tapering to less than 2 mm at the most basal level preserved. Transverse sections reveal sclerotic pith surrounded by a dictyoxylic stele with well-preserved xylem (Figs. 2, 3, 6). Phloem, endodermis, and parenchymatous inner cortex, like those that characterize living osmundaceous ferns, are incompletely preserved. However, such tissues are present in some frond bases (Figs. 5, 7). A sclerotic cortex surrounds the stele and is heterogeneous (Figs. 1–4, 6). All sclereids of the cortex are thick walled, but several layers of cells at the inner margin of the stem have thicker walls and smaller lumens than more peripheral cells (Fig. 6). Similar rings of thick-walled sclereids also are preserved around frond and root traces. Closely spaced frond bases and diverging roots enclose the rhizome (Figs. 1–3), producing an indistinct outer margin of the cortex (Figs. 2, 3). Longitudinal sections reveal that fronds diverge at angles of 40–45° (Fig. 4) and that adventitious root traces remain within the sclerotic frond base cortex for some distance beyond the margin of the stem.
Stem
The stem increases in diameter from less than 2 mm at the most proximal level preserved to more than 2 cm distally. The stem divides 2 cm from the base of the specimen, forming two steles distally (Fig. 8, at arrows). Although each branch is surrounded by diverging frond bases, both remain within a common sclerotic cortex for the length of the specimen preserved.
The stele is characterized by a prominent sclerotic pith (Figs. 2, 3, 6). At some levels cells of the pith are thick walled throughout (Figs. 3, 6), but at other levels there are thin-walled cells at the center (Fig. 2). Distal to the level of branching, cells are not preserved at the center of the pith (Fig. 8), suggesting that they were thin walled in life or immature at the time of fossilization. In cross sections the pith region is stellate (Figs. 2, 3, 6), a shape that results from large sclerotic bundles separating from the pith and diverging to the adaxial side of each leaf trace (Figs. 4, 6). In a series of sections through which a frond trace diverges, the pith first extends radially forming ribs and then each rib separates as a rod-shaped bundle near the adaxial surface of the frond trace. As each trace diverges through the cortex of the rhizome, the rod of sclerenchyma first becomes continuous with the sclerotic ring of the stipe (Fig. 6, at right), and then detaches from the ring to occupy the space within the C-shaped xylem bundle (Figs. 5, 7). Through the same distance the rod of sclerenchyma diminishes in radial thickness until it becomes a thin zone that lies adjacent to the C-shaped frond trace (Fig. 5, 7).
The stem stele consists of a small number of cauline bundles and diverging leaf traces throughout the length of the specimen. At the base, there are only three cauline bundles (Fig. 2, at arrows) and diverging leaf traces, but the number increases distally. At the level of Fig. 2, there are three frond traces diverging from the stele in a single section and about five orthostichies of leaves. More distally at the level of Figs. 3 and 6, the number of diverging traces has increased to four, and there are about 10 orthostichies. Above the level of branching, distortion and incomplete preservation make the number of cauline bundles and phyllotaxis difficult to determine (Fig. 8).
Cauline vascular architecture and leaf trace divergence
In a typical cross section of the rhizome, the stele includes both elliptical cauline bundles and C-shaped leaf traces, which are interconnected in various combinations (Fig. 6). Some leaf traces are not connected to a cauline bundle (Fig. 6, at right), while others have a cauline bundle attached either to the right or left side. A few traces appear to have a cauline bundle attached to each side (Fig. 6, at upper right). In addition, most sections show a root trace diverging from the periphery of a cauline bundle (Fig. 6, at left). These configurations are typical of osmundaceous ferns with dictyoxylic steles (Hewitson, 1962; Serbet and Rothwell, 1999).
Production of a leaf trace can be described from an acropetal series that begins at a level where a cauline bundle has no protoxylem strand (i.e., Fig. 6, at left). Progressing distally, a protoxylem strand appears in the bundle, and then the bundle becomes bilobed (Fig. 6, at upper left). The lobe with no protoxylem represents the cauline bundle, while the other lobe is the developing leaf trace. Continuing distally, the trace broadens tangentially, and metaxylem adaxial to the protoxylem strand diminishes in thickness. The leaf trace then becomes endarch and is clearly C-shaped (Fig. 6, at right). Distal to the level where the leaf trace separates from the cauline bundle, the cauline bundle fuses to an adjacent bundle/trace complex, thereby closing a leaf gap.
The single protoxylem strand located at the inner margin of the diverging leaf trace divides in two within the inner zone of the sclerotic cortex (Fig. 6, at right). The number of protoxylem strands continues to increase distally up to approximately six to eight at the level of frond divergence (Fig. 7, at arrowheads). Leaf trace metaxylem is typically one to two cell layers thick. It consists of tracheids that are 40–50 µm in diameter and that display scalariform secondary wall thickenings (Fig. 9).
Stipe bases
As is characteristic of living Todea barbara, cross sections of T. tidwellii reveal several stipes at various levels of divergence from the periphery of the rhizome (Figs. 2, 3), producing an irregular surface and obscuring the outer boundary of the cortex (Figs. 2, 3). Stipe bases are oval to elliptical in cross section and often distorted. The stipe bases are relatively isodiametric toward the outer margin of the rhizome cortex, broadening tangentially at the level of divergence (Figs. 2, 3). Individual stipe bases have a thin C-shaped xylem bundle (1–2 cells thick) with slightly recurved margins (Figs. 5, 7). There is a narrow space surrounding the xylem, that represents the position of phloem which otherwise is not preserved. The thin C-shaped sclerenchyma bundle occupies a position adjacent to the space on the concave adaxial side of the xylem (Figs. 5, 7). In some sections a layer of cells with prominent walls is preserved on the convex abaxial side of the vascular bundle (Fig. 7). Such cells are continuous with sclerenchyma of the cortex (Fig. 5), which is largely replaced by destructive calcite recrystallization. However, the preservation of a few patches of cells in this zone (Fig. 5) reveals that the cortical ring was originally composed of sclerenchyma throughout. Cortical sclerenchyma cells are 20–45 µm in diameter and have prominent lumens. There is a space between the leaf trace and the sclerenchyma ring like that which is occupied by parenchymatous ground tissue in living osmundaceous ferns (Hewitson, 1962; Bierhorst, 1971).
The sclerenchyma ring is heterogeneous, being distinctly thinner on the adaxial surface than in other areas (Figs. 2, 3, 5). It forms the outer margin of the stipe in all sections. There is no evidence of thin-walled paranchyma or lateral parenchymatous wings like those of other fossil and living osmundaceous species. Because of the calcite recrystallization of the sclerenchyma ring, we cannot be certain that lateral wings were absent in life.
Adventitious roots
As far as can be determined, one adventitious root trace diverges from the periphery of a cauline bundle in association with each frond trace (Figs. 4, 6). Root traces diverge from a cauline bundle (Fig. 6, at left), traverse the space between the stele and sclerotic cortex of the rhizome, and become surrounded by a ring of sclerenchymatous cells with small cell lumens (Fig. 6, at right). Roots extend obliquely toward the periphery of the trunk within the rhizome cortex and stipe bases (Fig. 4), eventually extending into the substrate from the abaxial surface of a stipe. There is complete histological continuity between the cortex of the rhizome and that of the root. Therefore, adventitious roots of T. tidwellii differentiated simultaneously with the other vegetative organs of the plant. Xylem of the roots is diarch, consisting of a plate of 6–8 tracheids in cross section (Figs. 3, 4).
Phylogenetic analyses
To test our hypothesis of generic affinities for T. tidwellii and of the broader phylogenetic relationships within Osmundaceae, we conducted a numerical cladistic analysis (maximum parsimony) using a combination of 1227 nucleotide sequences of the chloroplast gene rbcL (Yatabe et al., 1999) and 41 morphological characters (i.e., characters 1228–1268; Appendices 1, 2). The resulting tree was compared to results of previous phylogenetic analyses of the family (Figs. 10, 11). Results of this analysis yielded one most parsimonious tree of 1819 steps (CI = 54; RI = 51), that is identical to the results of Yatabe et al. (1999) except that T. tidwellii appears as the sister to T. barbara (Fig. 12). In this tree (Fig. 12) O. cinnamomea (i.e., Osmundastrum) is sister to the remaining Osmundaceae, and representatives of subgenera Osmunda and Plenasium (i.e., O. regalis + O. vachellii) form the sister group to a clade that includes the species of Todea and Leptopteris (i.e., L. hymenophylloides + [T. barbara + T. tidwellii]). Bootstrap support values for nodes on the tree range from 89 to 96% (Fig. 12).
DISCUSSION
Todea tidwellii consists of an anatomically preserved fern trunk with a dictoxylic rhizome and sclerenchymatous cortex. It has closely spaced frond bases with C-shaped traces that diverge in a helical phyllotaxis. This combination of characters is diagnostic for the filicalean family Osmundaceae (Hewitson, 1962; Miller, 1971; Tidwell and Ash, 1994). Within the Osmundaceae histological features of the trunks are characteristic of specific genera, and in some cases, even species (Hewitson, 1962; Miller, 1967, 1971; Serbet and Rothwell, 1999; Stockey and Smith, 2000). Whereas species of Osmunda have relatively uniform cortical sclerenchyma fibers that form a distinct outer surface of the rhizome, species of Leptopteris and Todea, including T. tidwellii (Fig. 3), have heterogeneous cortical sclerenchyma and an obscured outer margin of the rhizome (Hewitson, 1962). Species of Leptopteris have a parenchymatous pith, but Todea barbara and T. tidwellii have a sclerenchymatous pith. The rachis in species of Leptopteris displays a sclerenchymatous ring that is distinctly thicker than that of T. barbara. The sclerenchymatous ring of both T. papuana (Hennipman, 1968) and T. tidwellii is intermediate in thickness on the abaxial and lateral sides, but distinctly thinner on the adaxial side of the rachis (Fig. 5). This type of sclerenchymatous ring heterogeneity is not known to occur in other osmundaceous species.
Whereas T. tidwellii and species of both Osmunda s.l. and Leptopteris all display sclerenchyma in the adaxial concavity of the rachis trace, no sclerenchyma is present in that position in T. barbara (Hewitson, 1962) or T. papauana (Hennipman, 1968). In all other osmundaceous species where sclerenchyma is present abaxial to the leaf trace, it forms one or more bundles much thicker than the thin C-shaped band located at that position in T. tidwellii (Hewitson, 1962). Most osmundaceous rachides have scattered sclerenchyma within the parenchymatous tissue of the inner cortex, but this feature is absent from species of Leptopteris (Hewitson, 1962). Thin-walled ground tissue is not well enough preserved in T. tidwellii to determine the disposition of that feature. Another taxonomically useful character that varies among osmundaceous species is the distribution of sclerenchyma within the parenchymatous wings that occur at the base of the stipe (i.e., stipular wings). In T. tidwellii there is no evidence of stipular wings or of other parenchyma tissue outside the sclerenchymatous ring of the rachides. Although such wings may have been absent from T. tidwellii in life, their presence in virtually all other species of Osmundaceae suggests that absence may be due to incomplete preservation.
Systematics and phylogeny
The genus Todea is represented by the well-known species T. barbara and a second living species, T. papuana, which has been briefly described only once (Hennipman, 1968). Most features of T. papuana have not been characterized or critically compared to those of T. barbara and other osmundaceous ferns. The most distinctive known characters separating the two living species of Todea are differences in the sclerenchyma sheath surrounding the frond trace and sclerenchyma distribution within the stipular wings, but Hennipman (1968) also stresses that the latter character is highly variable at different levels with a single frond of T. papuana. Therefore, we are unsure whether more detailed studies of T. papuana will support segregation of such ferns at the species level, or if they will ultimately be regarded as falling within the range of variation that encompasses T. barbara. Because of a paucity of data, T. papuana was not included in the phylogenetic analyses.
Classical studies of osmundaceous ferns have established that living species conform to three genera Osmunda, Todea, and Leptopteris and that Osmunda s.l. may be further segregated to Osmunda L., Osmundastrum Presl., and Plenasium Presl. (Diels, 1898; Miller, 1967; Kramer, 1990). Most authors recognize Todea and Leptopteris as separate genera, but others favor including species of both within Todea (e.g., Hewitson, 1962). Whereas some authors recognize segregates of Osmunda as distinct genera, most consider them to be subgenera (Hewitson, 1962; Miller, 1967; Kramer, 1990). Except for O. claytoniana, which Miller regards as a member of subgenus Osmunda and Kramer (1990) recognizes as a species of Osmundastrum, species composition of the osmundaceous genera and subgenera are relatively uniformly agreed upon. Phylogenetic relationships among the living osmundaceous genera and subgenera have been less clearly understood (Miller, 1967, Miller, 1971; Kramer, 1990).
Miller (1971) was the first to employ phylogenetic systematics methods to resolve relationships among species of Osmundaceae. Using Wagner's Ground Plan/Divergence methodology (Wagner, 1969) Miller developed a set of 18 systematically informative morphological characters with at least two states each (Miller, 1971). Results of that analysis more or less supported the accepted segregation of living species into three genera (Osmunda, Leptopteris, and Todea), and resolved the three recognized subgenera of Osmunda s.l. However, T. barbara nested within a clade of Osmunda species, rendering the genus Osmunda a nonmonophyletic assemblage (Fig. 10). In that tree (Fig. 10), species of Leptopteris were least specialized and formed a clade that was the sister group to the remaining Osmundaceous species (Fig. 8 of Miller, 1971). Osmunda cinnamomea (subgenus Osmundastrum) plus T. barbara formed a small clade attached to the stem at the next more distal node, with remaining species of Osmunda resolving as two clades at the apex of the tree (Fig. 10). The latter included species of subgenus Osmunda (i.e., O. claytoniana, O. regalis, O. japonica, and O. lancea Thunb.) as the sister group to species of the subgenus Plenasium [i.e., O. vachellii, O. javanica l., O. bromeliaefolia (C. Prest.) Kuhn, and O. banksiaefolia (C. Presl) Kuhn].
More recently, Yatabe et al. (1999) assessed relationships among living osmundaceous species using nucleotide sequences of the chloroplast gene rbcL. Included in the analyses were representatives of each of the widely recognized osmundaceous genera and subgenera (i.e., Leptopteris hymenophylloides (A. Rich.) C. Presl., L. wilkesiana (Brack.) H. Christ, T. barbara, Osmunda japonica, O. lancea, O. regalis, O. claytoniana, O. cinnamomea, O. banksiaefolia, O. javancia, O. vachellii). One species of Ophioglossales, one species of Marattiales, and six species of other filicaleans were included as outgroups (Yatabe et al., 1999). Analyses were conducted using both maximum parsimony and neighbor-joining methodologies.
Results of the two analyses conducted by Yatabe et al. (1999) were concordant (Fig. 11) except for relationships among species of the subgenus Plenasium. As with the results of the Miller analysis (1971), Osmunda s.l. forms a nonmonophyletic assemblage (i.e., Fig. 1 of Yatabe et al., 1999), but the composition of the clade attached at the basal nodes of the tree differs from the results of Miller (1971) (Fig. 11). Whereas a Leptopteris spp. clade is attached at the basal node of the Miller (1971) tree and Osmunda cinnamomea + Todea barbara form a small clade attached to the stem at the next node, the Yatabe et al. (1999) results resolve Osmunda cinnamomea as sister to all other species of the family (Fig. 11). At the next more distal node of the Yatabe et al. tree, species of Leptopteris and Todea form a small clade that is the sister group to all of the remaining species of Osmunda s.l. Those results support Miller's recognition of O. cinnamomea as the only species of Osmundastrum, but contradict a basal position for Leptopteris within the osmundaceous clade (Fig. 11).
Our analysis used both the nucleotide sequence characters of Yatabe et al. (1999) and 41 morphological characters, most of which could be scored for all of the taxa (Appendix 1). The results of this analysis (Fig. 12) are fully concordant with those of Yatabe et al. (1999) (Fig. 11) except that T. tidwellii is added to the tree as the sister to T. barbara (Fig. 12). These results strongly support both the appropriateness of assigning T. tidwellii to the genus Todea and the accuracy of the Yatabe et al. tree. They also support segregating Osmundastrum (i.e., O. cinnamomea) to a separate genus (Table 1), as indicated by its location at the base of the tree that includes genera with living species (Fig. 12).
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The occurrence of sporangia on laminar pinnules that are similar to those of vegetative fronds in Todea and Leptopteris contrasts with fertile fronds (or frond segments) of Osmunda, which have narrow laminae that are highly reduced as compared to vegetative pinnules (Bower, 1926; Hewitson, 1962). This character has added to the perception that Todea and Leptopteris may be basal among living genera of Osmundaceae (e.g., Miller, 1971) because of their wide fertile pinnules. However, attachment of the Todea + Leptopteris clade at a node above Osmundastrum on the Yatabe et al. (1999) tree (Fig. 12) indicates that the common ancestor of living Osmundaceae could have borne sporangia on pinnules with highly reduced laminae. If the topology of the Yatabe et al. (1999) tree is accurate, then the laminar fertile pinnules of Todea and Leptopteris either represent a derived character among osmundaceous genera with living species or else narrow fertile pinnules evolved independently in O. cinnamomea and in the remaining species of Osmunda (Fig. 11).
Paleobiogeography of Osmundaceae
As early as the Late Permian, unequivocal osmundaceous species (sensu Phipps et al., 1998) were present in Australian Gondwana (Gould, 1970), with many species occurring in Australia, South America, Antarctica, Russia, and China by the Early Triassic (Cleal, 1993; Skog, 2001). This distribution suggests that the family originated on the Gondwana continent of the Southern Hemisphere during the Permian (Gould, 1970), spreading to the Northern Hemisphere through Asia and South America, and arriving in Europe and North America by the late Triassic (Skog, 2001). The origin of crown-group Osmundaceae by Late Triassic time (Phipps et al., 1998) suggests that some extant genera and species could be extremely ancient. If true, that would help explain the widely disjunct distributions of many living species (e.g., Hewitson, 1962; Yatabe et al., 1999). It also would account for the occurrence of Todea tidwellii in western North America, whereas restricted ranges of the two living species are half way around the world in New Zealand and New Guinea.
Calibration of clade ages for Osmundaceae
Osmundaceae and closely related ferns are represented by an unusually large number of morphospecies that range from the Late Permian, through the Mesozoic and Tertiary, and up to the present (Gould, 1970; Miller, 1971; Tidwell and Ash, 1994; Serbet and Rothwell, 1999; Stockey and Smith, 2000; Skog, 2001). More ancient dates for the clade (e.g., Schneider et al., 2004) remain unverified, either because they are calculated from inaccurate tree topologies (Rothwell and Nixon, 2006) and/or because the fossils have equivocal systematic relationships to modern Osmundaceae (i.e., Thamnopteridaceae sensu Miller, 1971).
Fossils of the Osmundaceae and the closely related family Guaireaceae Herbst form one of the most extensive paleontological records (Tidwell and Ash, 1994) for inferring evolution and phylogeny to be found anywhere among fern clades of the euphyllophytes (Rothwell, 1999). However, inferring the antiquity of crown group Osmundaceae from the paleontological record is complicated by almost all of the fossils being described as morphotaxa, rather than being understood as extinct species of plants. Up through the Jurassic, most morphospecies of compressed fertile osmundaceous fronds do not show synapomorphies for living genera (e.g., Todites Seward; Harris, 1961). Therefore, without knowledge about the rest of the sporophyte, those species cannot be assigned to a living genus with confidence. Likewise, most anatomically preserved osmundaceous trunks (Tidwell and Ash, 1994; Cantrill, 1997; Stockey and Smith, 2000) lack diagnostic features of living species, and little is known of their frond architecture, pinnule morphology, sporangia, or spores. Therefore, such fossils could represent either species of extinct genera or extinct species of genera with living representatives.
Compressed fertile frond segments described from the Late Triassic of Antarctica as Osmunda claytoniites Phipps, T N. Taylor, E. L. Taylor, Cuneo, Boucher & Yao (Phipps et al., 1998) provide the oldest unequivocal evidence for the genus Osmunda s.l., and establish a minimum age for crown group Osmundaceae of around 220 million years. Likewise, Todea tidwellii provides a minimum age of ca. 136 million years for the Todea clade. The earliest evidence for a living species of Osmundaceae consists of anatomically preserved trunks of Osmundastrum cinnamomea from the Campanian stage of the Upper Cretaceous (ca. 75 Ma [million years ago]; Lerbekmo and Braman, 2002) in western Canada (Serbet and Rothwell, 1999). That age establishes O. cinnamomea as having the greatest known species longevity of all vascular plants (Serbet and Rothwell, 1999).
Together, the minimum clade ages established by fossil Osmundaceae confirm hypotheses that the crown group evolved by the early Mesozoic, that the Todea+Leptopteris clade was present by the Early Cretaceous, and that living species began to appear no later than the Late Cretaceous. However, if the tree topology presented in Fig. 12 is accurate, then at least some of the Triassic morphospecies of Osmundaceae may actually represent the Osmundastrum clade. In this regard, we eagerly await the testing of these hypotheses by the future reconstruction of osmundaceous fossils as species of extinct plants and by the accurate placement of more fossil species on the phylogenetic tree.
Appendix 1. Matrix of scorings for states of morphological characters 1228 1268 as defined in Appendix 2.
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FOOTNOTES
1 The authors thank Drs. Y. Yatabe, Kyoto University, and H. Nishida, Chuo University, for providing their aligned nucleotide sequence matrix for phylogenetic analysis. They also are grateful to G. Cranham, T. Henrich, S. Hubbard, J. Morin, and M. Trask of the Vancouver Island Paleontological Society for collecting assistance. This work was supported in part by the Natural Sciences and Engineering Research Council of Canada (Grant A-6908 to R.A.S.) and by an Ohio University Provost Undergraduate Research Fund award (to N.A.J.). 
4 Author for correspondence (e-mail: rothwell{at}ohio.edu), phone: 740-593-1129
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