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Paleobotany |
2Department of Ecology and Evolutionary Biology and Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045-7534 USA; 3The New York Botanical Garden, Bronx, New York 10458 USA
Received for publication November 2, 2005. Accepted for publication February 27, 2006.
ABSTRACT
Cataphylls associated with the Middle Triassic stem genus Antarcticycas are described, and their impact on understanding cycad evolution is discussed. The cataphylls of Antarcticycas are triangular in outline and flattened adaxially with lateral flanges. The outer surfaces are covered with a ramentum of filamentous hairs, the epidermis is a single cell layer thick, and the ground tissue is parenchymatous with mucilage canals and sclereids. Vascular bundles form a distinct inverted omega-shaped pattern characteristic of the Cycadales observed in petioles of extant species. The structures in Antarcticycas are interpreted as cataphylls based on overall morphology, presence of straight vascular strands in the cortex of the associated stem, and lack of fascicular cambia in the vascular bundles. Because much of the overall diversity of Cycadales is represented by fossils, integrating fossil taxa into explicit phylogenetic hypotheses is important for understanding cycad evolution. Therefore, character and minimum age mapping were performed on a phylogeny of extant and fossil taxa including Antarcticycas. The results suggest that major extant lineages of Cycadales had diverged by the Permian to Triassic and that certain synapomorphies for Cycadales had evolved by the Permian. Evidence of insect feeding on Antarcticycas suggests that associations between cycads and insects are ancient.
Key Words: Antarctica • Antarcticycas • cataphyll • character evolution • Cycadales • minimum age mapping • phylogeny • Triassic
The extant Cycadales is a small group of gymnosperms with ca. 11 genera and 300 species distributed sporadically in tropical, subtropical, and warm temperate regions of the Americas, Africa, southeast Asia, and Australia (Jones, 2002
; Hill et al., 2004
). Cycads are the oldest and most primitive of the extant seed plant groups and thus are uniquely suited for exploring the origins of the earliest seed plants (Brenner et al., 2003
). However, much is still not understood about the cycads themselves. The history of the Cycadales spans over 250 million years with much of the reported overall diversity of the cycads represented by extinct taxa (e.g., Pant, 1987
). It has thus been surmised that the present diversity of the order is a relic of what was once a more diverse and/or more widely distributed group that reached the height of its development during the Mesozoic (e.g., Pant, 1987
; Kva
ek and Manchester, 1999
; Artabe et al., 2004
). If this hypothesis is correct, then it is only by understanding the fossil record of the group, and particularly the phylogenetic positions of the extinct taxa in relation to the extant taxa, that we can distinguish which features have contributed to the overall longevity and continued persistence of the Cycadales. Therefore, it is essential to understand the anatomy and morphology of extinct taxa, because this information can be used to incorporate fossil cycad taxa into explicit phylogenetic hypotheses in which both taxa and characters can be placed into evolutionary and temporal context.
Although the fossil record of the extant genera of Cycadales is concentrated in the Tertiary (Norstog and Nicholls, 1997
), it has been suggested that cycads were derived from Paleozoic pteridosperms (Mamay, 1969
, 1976
; Taylor, 1969
), and reports of Permian cycads have been published from both North America (Mamay, 1969
, 1973
, 1976
; however, see Axsmith et al., 2003
) and China (Zhu and Du, 1981
; Gao and Thomas, 1989a
, b). The fossil record of anatomically preserved cycad stems as identified by their synapomorphies with extant cycads (Table 1) begins in the Triassic and extends into the Tertiary with 12 named genera. The Triassic record is the richest with five genera, four from Upper Triassic sediments and the last from the Middle Triassic: Michelilloa Archangelsky et Brett (1963)
from Argentina; Vladiloxylon Lutz, Crisafulli, et Herbst (2003)
from Chile; Lyssoxylon Daugherty (Gould, 1971
) and CharmorgiaAsh (1985)
from the United States; and Antarcticycas Smoot, Taylor, et Delevoryas (1985)
from Antarctica.
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). Among characters that link Antarcticycas to modern cycads are the large pith and cortex of the stem (the ratio of pith to vascular tissue in Antarcticycas was given as 12 by Artabe et al., 2004
); "mucilage ducts in the ground tissue and associated with traces; poorly developed secondary vascular tissue with wide rays; scalariform-circular bordered pitting on the tracheids; and the horizontal course of tracheids within the cortex" (Smoot et al., 1985
, p. 1419). Antarcticycas was originally described as most similar to the extant genus Bowenia Hooker ex Hooker, which includes two species endemic to Australia (Hill et al., 2004
), in its anatomy; Bowenia and Antarcticycas are small subterranean plants with pith rays one or more cells wide and secondary wall thickenings marked by circular bordered to scalariform pits (Smoot et al., 1985
).
At the time of its initial publication, Antarcticycas was significant both in the extent of anatomical detail preserved and in its antiquity, as it demonstrated that typical cycad stem anatomy was present early in the Mesozoic and suggested that a squat growth habit may have originated earlier in cycad evolution than previously thought (Smoot et al., 1985
). In this paper, we expand the descriptions of Antarcticycas and its single species A. schopfii Smoot, Taylor, et Delevoryas, to include new material representing structurally preserved cataphylls and reevaluate the relationship of Antarcticycas to extant cycads and its bearing on our understanding of cycad evolution.
MATERIALS AND METHODS
Specimen preparation
The specimen described here (blocks 10123A, B; slide nos. 26289–26291) is preserved in permineralized peat collected from the Middle Triassic Fremouw Formation near Fremouw Peak, in the Beardmore Glacier area, Transantarctic Mountains, Antarctica (84°17'41''S, 164°21'48''E, 2385 m a.s.l.) (Barrett and Elliott, 1973
; Farabee et al., 1990
; Hammer et al., 1990
). The specimens of peat were cut into sections and the flat surfaces polished, then etched in 49% hydrofluoric acid. Peels of the etched surfaces were made using the acetate peel technique (Galtier and Phillips, 1999
). Peels were mounted on slides for study. Specimens are housed in the Paleobotany Division of the Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, under accession numbers 26289, 26290, and 26291. Slides of extant cycads were prepared using standard microtechniques and are housed in the collections at the New York Botanical Garden, Bronx, New York.
Specimens were photographed under reflected light using a Nikon (Tokyo, Japan) FinePix S1 Pro digital camera mounted on a copy stand (Figs. 1, 10); under reflected light using a Leica (Leica Microsystems GmbH, Wetzlar, Germany) DC500 digital camera attachment on a Leica MZ16 stereomicroscope (Figs. 2, 9, 11–14, 16), or with transmitted light using a Leica DC500 digital camera attachment on a Leica DM5000 B compound microscope (Figs. 3–8, 15, 17). Digital images were processed using Adobe Photoshop CS, version 8.0 (1999–2003, Adobe Systems).
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) are in plain type.
Cladistic analysis and character mapping
A cladistic analysis was performed using the matrix of morphological characters but excluding the chemical characters used to produce the Brenner et al. (2003
, fig. 2b) tree topology (Appendices 1, 2) with modifications to reflect newly described characters for Antarcticycas (Table 2). All fossil taxa included in the matrix have one or more features that definitively link them to Cycadales, allowing for evaluation in a phylogenetic context (Table 1). NILANBE is a composite terminal including characteristics of the organ taxa Nilssonia Brongn., Androstrobus Schimper, and Beania Carruthers, which Harris (1941)
suggested represent a single whole-plant genus.
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). One hundred replicates were performed starting from a random Wagner tree on which tree-bisection-reconnection (TBR) branch swapping was performed (mu*100;) holding up to 10 shortest trees per replicate (h/10;); once the replicates were complete, the shortest trees found were swapped to completion (max*;). The maximum number of shortest trees to be kept by NONA was limited to 10000 (h10000;), and the random seed was set to time (rs0;). The search sequence was "rs0; h10000; h/10; mu*100; max*;". Saved tree topologies were viewed, and characters were mapped using the WinClados interface in WinClada (Nixon, 1999–2002). All unsupported nodes (nodes with no character support) were collapsed in all most parsimonious trees.
Minimum age mapping
Minimum age mapping (Crepet et al., 2004
) was performed on the tree topology resulting from the analysis just described. The philosophy underlying the minimum age mapping method is that the minimum age of a node (divergence) must be at least as old as the oldest of its descendent lineages (see, for instance, the discussion in Nixon, 1996
). Although in its original conception, the method was used to place minimum absolute ages at nodes, these were not readily available for many of the fossil cycad taxa included in the tree, so we chose to apply relative ages instead. The age of first appearance in the fossil record was applied to taxa that persist through several geologic periods (or epochs, where those are known within the Tertiary), although several terminals were problematic. NILANBE, the composite terminal including Nilssonia, Androstrobus, and Beania, was ascribed to the Jurassic rather than Triassic because, although these genera occur in the Triassic (e.g., Ash, 2001
), the association among them was demonstrated for species from the Jurassic flora of Yorkshire (Harris, 1941
). The relative age of Fascisvarioxylon Jain is in question; originally described as Jurassic (Jain, 1972
), this genus may be Early Cretaceous in age (e.g., Drinnan and Crane, 1990
). Therefore, we chose a conservative approach and applied a Cretaceous age to the genus.
Minimum age mapping is not exhaustive with respect to all reports of fossils representing extant genera; rather, preference was given to reports of fossils where diagnostic features (for instance, cuticle) were preserved. In several cases, including Zamia L. and Ceratozamia Brongn., the fossil taxa were described in the early to mid-20th century and have not been sufficiently reinvestigated since (Hollick, 1932
; Brown, 1962
). The ages of Zamia and Ceratozamia should thus be considered provisional pending reinvestigation of the identity of fossils on which they are based. Although the report of species of Dioon Lindley, like that of Ceratozamia, was originally made by Hollick in 1932, reinvestigation of the material by Moretti et al. (1993)
suggested that the fossil taxa could represent part of the stem lineage of the extant genus on the basis of the type of leaflet vein anastomoses and the type of leaflet insertion on the rachis preserved in the fossil specimens, which are synapomorphies for Dioon. Thus, this report of Dioon is considered valid. While originally described as Eocene by Hollick (1932)
, a more recent interpretation of the composition of the Hamilton Bay flora (Kootznahoo Formation), Kupreanof Island, Alaska, from which fossils of both Dioon and Ceratozamia were originally described, suggest it may be Paleocene in age (J. A. Wolfe, U. S. Geological Survey (USGS), 1963, written communication excerpted in Latham et al., 1965
, p. R31). Wolfe (1963, in Latham et al., 1965
) also made another report of D. praespinulosumHollick (1932)
from the Paleocene Little Pybus Bay flora (Kootznahoo Formation), Admirality Island, Alaska.
Citations for all relative ages used in minimum age mapping are given in Table 3. Absolute ages cited in the discussion of the minimum age mapping results after Gradstein et al. (2004)
refer to the absolute age assigned to the more recent boundary of each relative age interval (period or epoch). These absolute ages may not reflect more ancient absolute ages ascribed to specific fossil-bearing strata.
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One most parsimonious tree of length 153 steps, consistency index (CI) 0.62, retention index (RI) 0.75, including four uninformative characters, was found. The topology of the tree is the same as the topology of the tree published by Brenner et al. (2003)
for Cycadales, although the outgroup clade including Nilssoniocladus Kimura et Sekido, Mesospermae, and Ginkgoales and the ingroup clade including Zamia, Microcycas A. DC, and Chigua Stevenson are each less resolved.
SYSTEMATICS
Genus
Antarcticycas Smoot, Taylor, et Delevoryas emend. Hermsen, T. N. Taylor, E. L. Taylor, et Stevenson.
Generic diagnosis
Stems with central parenchymatous pith, weakly developing ring of endarch vascular bundles separated by large rays and parenchymatous cortex. Vascular bundles of secondary xylem and phloem containing uni- to triseriate rays. Mucilage canals present in both pith and cortex. Primary xylem with helical-scalariform secondary wall thickenings; secondary xylem tracheids with circular bordered pits. Traces extending through large rays, often accompanied by a mucilage canal. Within cortex, traces either proceeding straight to periphery of stem or turning sharply and extending horizontally to produce girdling configuration. Outer surface of stem irregular, covered with amorphous material containing remnants of cell walls. Cataphylls roughly triangular in transverse section with long lateral flanges; vascular bundles forming an inverted omega-shaped pattern.
Type species
Antarcticycas schopfii Smoot, Taylor, et Delevoryas, 1985
Species
Antarcticycas schopfii Smoot, Taylor, et Delevoryas emend. Hermsen, T. N. Taylor, E. L. Taylor, et Stevenson.
Specific diagnosis
Stems circular in transverse section, up to 4.0 cm in diameter. Parenchymatous pith and cortex containing scattered cells with dark contents. Mucilage canals ramifying throughout cortex and present in two zones, one at the periphery of the pith and another just outside the region of vascular tissue in the inner cortex. Ring of vascular bundles up to 7 mm thick, consisting of secondary xylem tracheids, cambial zone, and secondary phloem. Secondary phloem of thin-walled sieve cells with elliptical sieve areas, alternating with zones of crushed cells. Tracheids rectangular in cross section with crowded alternate, circular bordered pits. Traces composed of scalariform tracheids, continuous with tracheids of both primary and secondary xylem. Stem delimited by layer of periderm. Cataphylls sometimes present surrounding stem tissue, tightly arranged, interrupted by adventitious roots and separated from one another by dense layers of filamentous hairs; cataphyll shape roughly triangular in transverse section with long, lateral flanges, adaxial side flat; dense indumentum of sinuous hairs interpreted as covering both adaxial and abaxial surfaces; epidermis one cell layer thick; mesophyll of undifferentiated parenchymatous cells with sporadic sclerenchymatous cells and mucilage ducts; vascular bundles collateral; xylem of tracheids with scalariform thickenings. Roots diarch to polyarch with parenchymatous cortex; larger roots with secondary xylem and periderm layer.
Holotype
Specimen 568 (Smoot et al., 1985
, figs. 3-8, 10–14, 16, 19, 20).
Formation
Fremouw Formation, Beacon Supergroup.
Age
Middle Triassic
Type locality
Collected north of Fremouw Peak, Queen Alexandra Range, Antarctica (84°17'41''S, 164°21'48''E, 2385 m a.s.l.), Buckley Island Quadrangle (Barrett and Elliott, 1973
).
Repository
All specimens are housed in the Paleobotany Division of the Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas, USA.
Description of cataphylls
The cataphylls are found in association with stem tissue of Antarcticycas and are interrupted by adventitious roots characteristic of the genus. Although the particular stem with which the cataphylls are associated is partial and its vascular cylinder is not preserved, several histological features characteristic of Anarcticycas (e.g., an outer periderm, large cortex with mucilage canals, and leaf traces traversing the cortex horizontally) indicate that they belong to the same taxon (Fig. 1). Overlapping cataphylls surround the stem tissue. Each cataphyll is roughly three-sided in transverse section, with a flattened adaxial surface and long lateral flanges (Figs. 1, 2); cataphylls are approximately 13–17 mm wide by 1.5–4 mm in height (x = 4). The spaces between each of the cataphylls are ca. 0.20–1.06 mm thick and filled with numerous unicellular sinuous hairs that form a ramentum on the outer surfaces of each of the cataphylls (Figs. 4, 8).
The epidermis of each cataphyll is thin, composed of single layer of cells that appear oblong in transverse section (Fig. 5). The ground tissue is primarily composed of thin-walled undifferentiated cells, though some thick-walled cells are scattered sporadically among them (Fig. 6). Roughly circular to elongate mucilage canals occur within the ground tissue; these are up to 0.86 mm wide on their longest axes in transverse section (Fig. 2). Collateral vascular bundles up to 0.54 mm in diameter (although many have been peeled at what appears to be a slightly oblique angle) are arranged in an inverted omega-shaped pattern within the ground tissue (Fig. 2). Bundles are arranged with a poorly preserved zone of cells interpreted as representing the phloem oriented approximately to the abaxial side of each cataphyll; xylem is adaxial (Figs. 2, 3). Tracheids have scalariform thickenings (Fig. 7).
Insect-feeding galleries with associated coprolites traverse the cataphyll tissue (Fig. 9). These galleries are irregular in course with smooth walls. They traverse trichomes, epidermal tissue, and ground tissue (Fig. 9).
DISCUSSION
Cycads produce three classes of foliar organs—sporophylls, cataphylls or scale leaves (Figs. 10–15), and foliage leaves (Figs. 16–17); these differ from one another not only morphologically but also anatomically, specifically with respect to the vasculature (Matte, 1904
; Stevenson, 1990
). Foliage leaves are vascularized by girdling traces arising from the stele, and the pattern of the vascular bundles in the petiole or rachis in transverse section forms an inverted omega shape (Fig. 16); the bundles are very well developed, and each one has a distinct fascicular cambium (Fig. 17). In contrast, the traces to the cataphylls are not girdling, and the pattern of the vascular bundles in transverse section is either an indistinct inverted omega or a straight line (Figs. 11, 12); the bundles are poorly developed, and each lacks a fascicular cambium (Fig. 15). The sporophyll traces are also nongirdling, and the pattern of the vascular bundles in transverse section is a straight line; there are only 1–3 bundles at the base of each sporophyll, each quite well developed with an active fascicular cambium. These anatomical features make it easy to accurately distinguish among the three types of lateral appendages.
The structures described here with the stem tissue of Antarcticycas have vascular bundles which form a well-developed inverted omega-shaped pattern (Fig. 2). This may suggest they represent petioles rather than cataphylls; however, our interpretation that they are cataphylls is based on several other morphological and anatomical similarities to cataphylls. The structures are flattened in shape in transverse section with elongated lateral flanges and highly wrinkled outer surfaces (Figs. 1, 2), appearing more similar to cataphylls (Figs. 10–12, 14) than petioles (Fig. 16) when compared with both structures in extant cycads. Petioles tend to be terete to rhomboidal in transverse section (Fig. 16), and those of extant taxa observed here had less pronounced wrinkling of the outer surfaces than did some of the cataphylls (Figs. 10–12, 14). The Triassic structures have a dense indumentum of filamentous sinuous trichomes (Figs. 4, 8) similar to those characteristic of modern cycads (Figs. 13, 14). While emerging leaves of cycads also have a dense indumentum, hairs are lost as the leaves mature (Stevenson, 1981
). Furthermore, although girdling traces have been described from stems of Antarcticycas, the vascular strands in the cortex of the stem associated with the structures are straight (Fig. 1). Finally, the vascular bundles within the cataphylls of Antarcticycas are relatively small and have no evidence of a well-developed fascicular cambium (Figs. 2, 3), more similar to vascular bundles of cataphylls (Figs. 11, 12, 15) than those of petioles (Figs. 16, 17) in extant cycads.
While the possibility that these structures represent petioles rather than cataphylls cannot be completely eliminated without knowing their overall form, their morphology and anatomy in transverse section, except for the distinctness of the inverted omega-shaped pattern of the vascular bundles, strongly suggest that they are cataphylls.
Other fossil cataphylls
Cataphylls have been described attached to several other fossil cycad stems. Ash (1985)
described cataphylls attached to the stem of the Triassic taxon Charmorgia dijolii Ash. He illustrated the anatomy of both petioles and cataphylls of Charmorgia, describing the petioles as having a well-developed inverted omega-shaped pattern of vascular traces and the cataphylls a more poorly developed pattern, similar to those in the extant genus Cycas L. The cataphyll bases of Charmorgia are similar to the cataphyll bases preserved in Antarcticycas in that they also have wrinkled upper and lower surfaces, mucilage ducts, ground tissue primarily composed of parenchyma but with some thick-walled cells, a single-layered epidermis, and a ramentum of unbranched hairs. They differ primarily in the pattern of the vascular bundles, with the inverted omega pattern more poorly developed in cataphylls of Charmorgia than in cataphylls of Antarcticycas.
Cataphylls have also been reported on the compressed Triassic genus Leptocycas Delevoryas et Hope (1971)
from the United States, the Cretaceous genera Brunoa Artabe, Zamuner, et Stevenson and Worsdellia Artabe, Zamuner, et Stevenson from Argentina (Artabe et al., 2004
), and ambiguously from the structurally preserved Late Jurassic/Early Cretaceous stem genus Fascisvarioxylon Jain from India (Jain, 1962
, 1972
; Drinnan and Crane, 1990
). The anatomy of the cataphylls in these taxa was not described.
Plant–insect interactions
Some of the cataphylls of Antarcticycas exhibit evidence of insect feeding, including what appear to be feeding traces in the tissue and abundant coprolites (Fig. 9). Extant cycads are insect-pollinated, particularly by beetles (especially weevils) that feed on the microsporophylls, become covered in pollen, and then are attracted to female cones (Chadwick, 1993
; Connell and Ladd, 1993
; Fawcett and Norstog, 1993
; Norstog et al., 1993
; Ornduff, 1993
; Norstog and Nicholls, 1997
; Stevenson et al., 1998
). There have been no microsporangia found in association with the cataphylls described here, so it is unclear whether the predation of these cataphylls is connected with the pollination biology of Antarcticycas. There are also a number of insects that are parasitic on cycads although not known to be involved in pollination, especially lepidopterans; however, the earliest undisputed lepidopteran fossils do not appear until the Jurassic (Norstog and Nicholls, 1997
; Grimaldi and Engel, 2005
). Klavins et al. (2003
, 2005
) also reported coprolites in isolated cycad pollen sacs that occur in association with the microsporangiate cone Delemaya Klavins, Taylor, Krings, et Taylor, the only other cycad taxon known from the Triassic of Antarctica and possibly representing the pollen cone of Antarcticycas, although the two taxa have not yet been found in attachment. The coprolites in pollen sacs associated with Delemaya are composed entirely of pollen (Klavins et al., 2003
, 2005
), whereas those in the Antarcticycas cataphylls are not. In extant cycads, some pollinating insects consume pollen and some do not (Norstog and Nicholls, 1997
; Stevenson et al., 1998
), so the composition of the coprolites does not necessarily shed light on the ecological relationship of the insects feeding on the cataphylls to Antarcticycas.
Phylogenetic implications
Cataphyll characters, other than their presence or absence on vegetative or reproductive axes, have not been considered of great importance in reconstructing cycad relationships (Stevenson, 1990
; however, see de Laubenfels, 1999
). However, the genus Antarcticycas as a whole, including the newly described cataphylls, possesses a number of anatomical characters that may be phylogenetically significant. A cladogram of fossil and extant cycad taxa based on morphological data suggests that, of the 17 terminals representing fossil cycad taxa in the tree, only two Triassic taxa, Michelilloa and Antarcticycas, group outside of the clade including all extant cycads (Fig. 18). These two taxa lack cone domes, whereas presence of cone domes is a synapomorphy uniting the remainder of the cycads, with a later reversal to the "primitive" state of this character uniting Charmorgia, Bororoa Petriella, Menucoa Petriella, Fascisvarioxylon, Encephalartos Lehm., Lepidozamia Regel., and Macrozamia Miq. (Fig. 18). This suggests that lack of cone domes is both a primitive character (pleisiomorphic for the Cycadales) and also a derived character through loss. Michelilloa is further separated from the remainder of the cycads on the tree by the amount of wood parenchyma (Fig. 18), scanty in Michelilloa but abundant in Antarcticycas and the majority of other cycad taxa in which the amount of wood parenchyma is known, including all extant taxa except Dioon (Greguss, 1968
).
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; Hill et al., 2003
; Rai et al., 2003
; Bogler and Francisco-Ortega, 2004
; Chaw et al., 2005
), but appears similar in topology to at least some of the analyses based on morphological data from extant genera alone (Stevenson, 1990
; Brenner et al., 2003
; however, see Schutzman and Dehgan, 1992
) with regard to the relationships among the extant taxa. It should be noted, however, that while molecular data sets generally agree in the separation of Cycas from the remainder of the extant Cycadales and in a nonsister relationship between Bowenia and Stangeria, they have yet to converge on a single, stable set of relationships among extant cycad taxa (Treutlein and Wink, 2002
; Hill et al., 2003
; Rai et al., 2003
; Bogler and Francisco-Ortega, 2004
; Chaw et al., 2005
). Furthermore, relatively sparse sampling of the extant genera in some analyses (Rai et al., 2003
), rooting within the ingroup (Bogler and Francisco-Ortega, 2004
; Chaw et al., 2005
), and lack of resolution in consensus trees (Treutlein and Wink, 2002
; some trees in Hill et al., 2003
), make it difficult to compare results among papers or to draw conclusions as to trends in character evolution from these studies at this time.
While Smoot et al. (1985)
suggested the features preserved in the root and stem material of Antarcticycas make it most similar to the modern genus Bowenia among extant cycads (although a direct relationship was not necessarily implied), the features preserved in the new material render this comparison questionable. Both morphological and molecular data sets suggest that Bowenia may be relatively derived within the Cycadales (Stevenson, 1990
; Brenner et al., 2003
; Hill et al., 2003
; Rai et al., 2003
; Bogler and Francisco-Ortega, 2004
; Chaw et al., 2005
; Fig. 18), whereas the characters preserved in specimens of Antarcticycas appear to be primitive among the extant genera, especially when mapped on topologies including both extant and fossil taxa. The position of Antarcticycas in the tree based on morphological data, in fact, would suggest that Antarcticycas is not particularly close to any of the extant genera (Fig. 18). Although the new characters provided in this paper were added to the matrix used to construct the Brenner et al. (2003)
tree topology (Table 2; Appendices 1, 2), the characters did not alter the relationships among members of the Cycadales found in the original tree because the newly coded characters, including trichome, cataphyll, and petiolar characters (through inference), are pleisiomorphic within the Cycadales. In fact, all features coded for Antarcticycas, except the abundant wood parenchyma, which separates it from Michelilloa, appear to be primitive within Cycadales. Some primitive features of significance in the context of overall cycad evolution and/or a possible Antarcticycas-Bowenia connection preserved in Antarcticycas stems, roots, and cataphyll bases include a lack of cone domes (already discussed), a monoxylic stem, inverted omega shape of the pattern of vascular bundles in the petioles (as inferred from the pattern in the cataphylls), lack of specialized trichomes, and absence of cortical steles (Fig. 18).
Although very few anatomically preserved cycad stem taxa are known from the fossil record, it is interesting that the oldest, including all five Triassic genera, are monoxylic (Artabe et al., 2004
). Not until the Cretaceous does centrifugal polyxylic stem anatomy definitely appear, and at least three out of four of the Cretaceous genera have it, including Brunoa, Worsdellia, and Sanchucycas Nishida, Nishida, et Tanaka, whereas Centricycas Cantrill is ambiguous and Fascisvarioxylon, which may be Jurassic or Early Cretaceous in age, lacks centrifugal polyxyly (Nishida et al., 1991
; Cantrill, 2000
; Artabe et al., 2004
; the Jurassic age of Fascisvarioxylon modified from Jain, 1972
, after Drinnan and Crane, 1990
). The Cretaceous–Tertiary genus Bororoa and the Tertiary genus Menucoa are also characterized by centrifugally polyxylic stems (Petriella, 1969
, 1972
, 1978
; Artabe et al., 2004
). Among extant taxa, centrifugal polyxyly occurs in Encephalartos, Lepidozamia, Macrozamia, and Cycas L. Only Fascisvarioxylon has a ring of centripetal xylem, although some centrifugally polyxylic taxa have centripetal bundles. While Artabe and Stevenson (1999)
suggested that Permian fossils similar to modern Cycas render the assumption of monoxyly as the pleisiomorphic state of the cycadalean stem questionable, optimization of this character on the topology in Fig. 18, which shows Cycas as sister to the remainder of the extant Cycadaleans, suggests that monoxyly is the primitive state for the group.
A modified inverted omega-shaped or circular pattern of vascular bundles (as opposed to an inverted omega-shaped pattern) in the petiole was a synapomorphy uniting the taxa Bowenia and Stangeria in trees based on morphological data in Stevenson (1990)
. Stangeria is here coded as having an inverted omega pattern of vascular bundles (Appendix 1), making the modified omega-shaped pattern of vascular bundles autapomorphic for Bowenia with independent derivations in Bororoa and Encephalartos on the single most parsimonious tree (Fig. 18). Similarly, the modified omega pattern appears to have evolved through two independent derivations when mapped on some topologies suggested by molecular data (Hill et al., 2003
; Bogler and Francisco-Ortega, 2004
; Chaw et al., 2005
). Although the petiole traces were not directly observed in Antarcticycas, they are inferred to be similar in their pattern to the cataphyll bundles, which have the pleisiomorphic inverse omega-shaped pattern of the Cycadales (Fig. 18).
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). Branching trichomes are found in Cycas, Zamia, Microcycas A. DC., and Chigua Stevenson, equally branched trichomes in Zamia, Microcycas, and Chigua, and short, curved, colored trichomes in Bowenia, Macrozamia, and Lepidozamia (Stevenson, 1981
, 1990
). Based on the trees shown in Stevenson (1990)
, Brenner et al. (2003)
, and in Fig. 18, equally branched trichomes may be a derived character linking Zamia, Microcycas, and Chigua, whereas curved trichomes must have arisen at least twice on the most parsimonious trees (Chigua was not included in the Stevenson [1990]
analysis). Interestingly, in some topologies suggested by molecular sequence data, Bowenia groups within a clade containing Encephalartos, Lepidozamia, and Macrozamia rather than with Stangeria, suggesting that curved trichomes may have arisen only once with a reversal in Encephalartos (Hill et al., 2003
). Under either scenario of relationships, the presence of branched, equally branched, or curved trichomes appears to be apomorphic within the Cycadales. Antarcticycas lacks these trichome types, instead having long filamentous unicellular trichomes that are unbranched, similar to those that have been documented from nearly all the extant cycad genera (Stevenson, 1981
). While these trichomes are two-celled in extant cycads, with a bulbous basal cell and filiform apical cell, the presence of a basal cell could not be confirmed in Antarcticycas (Stevenson, 1981
; Figs. 4, 8).
Finally, Antarcticycas lacks cortical steles, while Bowenia has them. Interestingly, cortical steles have a pattern of distribution somewhat similar to curved trichomes among extant cycads. They are present in Encephalartos, Lepidozamia, and Macrozamia, uniting them into a clade in tree topologies suggested by morphological data, and they are also present in Bowenia and Cycas (Stevenson, 1981
, 1990
; Brenner et al., 2003
; Fig. 18). Under those sequence-data-based topologies where Bowenia groups with Encephalartos, Lepidozamia, and Macrozamia (Hill et al., 2003
), this would indicate that cortical bundles had only two originations, whereas scenarios suggested by morphological data alone indicate they had three. In this study, Anarcticycas has the pleisiomorphic state, and the recently described stem genus Worsdellia is the only fossil cycad taxon from which these bundles have been described (Artabe et al., 2004
).
Smoot et al. (1985)
postulated that the presence of both Leptocycas (Delevoryas and Hope, 1971
), with a treelike habit, and Antarcticycas, with a squat, subterranean habit, in the Triassic may indicate that there were two lines of cycad evolution, one represented by small, squat forms such as Bowenia and Stangeria and another represented by large, tree-like forms, and that this split occurred early in the history of the Cycadales. Neither molecular nor morphological phylogenetic analyses currently support this interpretation, though for different reasons. As noted earlier, molecular studies suggest that Bowenia and Stangeria are not closely related, although they are similar in several morphological and anatomical features (Stevenson, 1990
, 1992
). The tree produced by the only morphological analysis including Antarcticycas, while placing Bowenia and Stangeria together, places Antarcticycas outside of the extant taxa and thus suggests a more complex scenario in the evolution of these different habits (Brenner et al., 2003
; Fig. 18). Furthermore, all extant genera with more than three species have multiple growth forms, from subterranean species to species with squat, bulbous stems to arborescent species with large trunks (Stevenson, 1990
).
Age of the Cycadales
While Cycadales have long been thought to have originated from Paleozoic pteridosperms (Mamay, 1969
, 1976
; Taylor, 1969
) and fossils comparable to the modern genus Cycas date to the Permian (Gao and Thomas, 1989b
), fossil cycads assigned to extant genera are known primarily from the Tertiary (e.g., Hollick, 1932
; Hill, 1978
, 1980
; Carpenter, 1991
). A recent study based on rbcL sequence divergences suggests that the extant Cycadales is a young group relative to the postulated antiquity of cycads in general. Treutlein and Wink (2002)
dated divergences among members of the extant Cycadales using rbcL sequence data from extant cycads calibrated with land plant divergence times after those used in Savard et al. (1994)
; they calculated the divergences under a molecular clock. Based on their results, they hypothesized that extant Cycadaceae sensu Stevenson (1990)
and Zamiaceae sensu Stevenson (1990)
had split at the earliest ca. 92.5 million years ago (Ma), or in the Late Cretaceous, and that the divergence between Encephalartos and the Macrozamia-Lepidozamia lineage likely occurred in the Neogene, with the African disjunction of Encephalartos from the two Australian genera due to Miocene long-distance dispersal rather than continental drift.
Taking a different approach, we applied Crepet et al.'s (2004)
minimum age mapping method to the tree topology including both extant and fossil taxa and based on morphological data (Fig. 19). The results of the minimum age mapping method are quite different from those of the rbcL divergence study. Based on minimum age mapping applied to the topology in Fig. 19, the initial divergence among the lineages leading to the extant Cycadales dates at least to the Permian; in other words, this divergence is at least 251 million years old according the most recent Geologic Time Scale (Gradstein et al., 2004
). The Cycas lineage also appears to have diverged from the remainder of the extant Cycadaleans by that time. Furthermore, if the tree topology in Fig. 19 is accurate, it suggests that the four remaining extant cycad lineages had diverged from one another by the Triassic, or more than ca. 199 Ma according to the Gradstein et al. (2004)
time scale. Finally, Encephalartos appears to have split from the Lepidozamia-Macrozamia lineage no later than the Eocene, minimally at ca. 45 Ma based on a K-Ar date associated with the deposits from which specimens of Lepidozamia were collected (Hill 1978
, 1980
). Rai et al. (2003)
noted that the chloroplast regions examined in their study, which included rbcL, appear to be highly conserved in the extant cycads in comparison to most other extant seed plant groups. This may help to explain what appear to be the anomalously recent dates of divergence found in the study by Treutlein and Wink (2002)
when compared to the minimum age mapping method.
|
). This appears to be concordant with the finding here that the Cycas lineage may have diverged from the other extant lineages no later than the Permian. Moretti et al. (1993)
also suggested that the extant genus Dioon is over 60 million years old based on an evaluation of the taxon's biogeography in comparison to a phylogeny suggested by restriction fragment length polymorphisms (RFLPs). Their conclusion is plausible in the context of the minimum age mapping results, which only suggest that the lineage leading to Dioon diverged from the Lyssoxylon lineage no later than the Triassic; Dioon itself is first identified from Paleocene deposits, meaning the genus is at least 55 million years old (J. A. Wolfe, USGS, 1963, excerpted in Latham et al., 1965
, p. R31; Gradstein et al., 2004
). Treutlein and Wink's (2002) results, in contrast, suggest that Dioon may have diverged as recently as the Miocene (based on the minimum of the divergence times calculated between species of Dioon and species within other genera of Cycadales; Table 1 in Treutlein and Wink, 2002
).
While it is possible that divergences among the lineages represented by the extant genera of cycads are quite ancient, others have suggested that the species within extant genera may have diversified more recently, within the Cenozoic (Moretti et al., 1993
; Treutlein and Wink, 2002
). Unfortunately, infrageneric divergence times cannot be evaluated in the context of the current phylogeny. Rather, infrageneric phylogenies incorporating fossils identified as belonging to extant genera, as well as those identified as representing sister taxa to extant genera in this analysis, are necessary both to determine the monophyly of extant genera with respect to their extinct sister taxa and to explore the timing of diversification within extant groups.
Conclusions
The attributes of Antarcticycas, as a whole, lend credence to the idea that the Cycadales is a group that has maintained remarkable stasis through time. This study has demonstrated that Antarcticycas schopfii, the earliest known structurally preserved cycad taxon, possesses a number of features apomorphic to the Cycadales. Among the autapomorphies of Cycadales (Table 1), Antarcticycas was already known to possess girdling leaf traces (Smoot et al., 1985
) and through inference has been shown to possess an inverted omega-shaped pattern of the petiole vascular bundles (Fig. 2). Based on minimum age mapping combined with mapping of the origin of these features on a phylogeny of the Cycadales (Fig. 19), this would suggest that girdling leaf traces and the omega-shaped pattern of the vascular bundles had both evolved no later than Permian, indicating that the Cycadales were well differentiated from other seed plant groups by that time and possessed at least some of their characteristic modern attributes. The position of Antarcticycas in the phylogeny shown in Figs. 18 and 19 suggests that it may be its own evolutionary offshoot, rather than a direct ancestor of the modern cycads; this is because Antarcticycas is younger than the most recent common ancestor of the clade including all of the extant cycads (which is at least Permian in age), yet it diverges from the remainder of the Cycadales prior to the appearance of this ancestor (Fig. 19). In contrast, other Permian and Triassic taxa except for Michelilloa are both more derived than Antarcticycas and are nested among the extant Cycadales (Fig. 19).
This study represents an important step in bringing together knowledge of extinct and extant cycad taxa in order to understand both the timing of diversification events within the Cycadales as well as the relative order and timing of appearance of particular cycad traits. However, the current study largely incorporates Mesozoic fossil taxa, whereas the record of fossils assigned to extant cycad genera is concentrated in the Tertiary (e.g., Brown, 1962
; J. A. Wolfe, USGS, 1963, excerpted in Latham et al., 1965
, p. R31; Hill, 1978
, 1980
; Carpenter, 1991
). Incorporation of more Tertiary fossils, including taxa within and outside of extant genera, as well as further sampling of extant species, is especially relevant to understanding the continued endurance of extant cycad taxa and what is thought to be the relatively recent infrageneric diversification of some of these taxa, which has been attributed to various factors such as response to successive vicariance events (Moretti et al., 1993
, for Dioon) or the evolution of weevil pollination (Oberpreiler, 2004; however, see Brenner et al., 2003
). Only by placing the anatomical and morphological traits of the cycads into phylogenetic and temporal context can we hope to make progress in understanding the longevity of this group.
|
1 NSF grant OPP 0229877 to T. N. and E. L. Taylor provided funding for this research. 
4 Author for correspondence (ehermsen{at}ku.edu
)
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