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Paleobotany |
2Department of Geological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 USA; 3Botanical Museum, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138 USA; 4Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences, Nanjing 210008, People's Republic of China; 5Department of Biological Sciences, State University of New York, Binghamton, New York 13901 USA
Received for publication March 11, 2003. Accepted for publication October 7, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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Key Words: Corallinales • Florideophyceae • Neoproterozoic • Rhodophyta • South China
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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), and scattered fossils in Paleozoic rocks preserve an earlier record of calcifying reds (Brooke and Riding, 1998
). Apparent bangiophyte fossils in ca. 1200 Myr cherts from Arctic Canada, however, imply a much earlier divergence of rhodophyte clades (Butterfield, 2000
). In this paper, we discuss anatomically preserved fossils from the late Neoproterozoic Doushantuo Formation, China, that help to bridge the stratigraphic and evolutionary gap between the earliest rhodophyte fossils and the calcified red algae in much younger rocks.
Doushantuo deposits preserve a remarkable diversity of macro- and microorganisms as petrifications in early diagenetic cherts and phosphorites, as well as carbonaceous compressions in contemporaneous black shales. Cellularly preserved cyanobacteria, acritarchs, algae, and microscopic metazoans have all been described from Doushantuo phosphorites at Weng'an (Guizhou Province) and elsewhere in South China (Xiao et al., 1998
, 1999
, 2000
; Yuan and Hofmann, 1998
; Zhang et al., 1998
; Yin, 1999
, 2001
; Yin et al., 2001
; Zhou et al., 2001
, 2002
; Yuan et al., 2002
). Our focus here is on phosphatized multicellular algae that have been interpreted as rhodophytes. Previous studies of Weng'an algal fossils were based mostly on observations of randomly oriented thin sections, making it difficult or impossible to understand the three dimensional morphology of these remains. Nonetheless, previous researchers were able to delineate taxa and suggest broad rhodophyte affinities for Weng'an thalli (Zhang, 1989
; Zhang and Yuan, 1992
, 1996
; Xiao et al., 1998
; Yuan and Hofmann, 1998
; Zhang et al., 1998
).
In this paper, we report new fossil populations from Doushantuo phosphorites at Weng'an, including algal thalli isolated from rock matrix using acid maceration techniques. We observed carefully oriented thin sections of isolated fossils, as well as randomly oriented sections of fossils embedded in the rock matrix. These materials provide new insights into the morphology and, possibly, the reproductive biology of Doushantuo thalli. Together with recent advances in rhodophyte phylogeny (Freshwater et al., 1994
; Ragan et al., 1994
; Saunders and Kraft, 1997
; Harper and Saunders, 2001b
; Müller et al., 2002
) and a new conceptual framework for the phylogenetic interpretation of fossils (Jeffries, 1979
; Runnegar, 1996
; Budd and Jensen, 2000
), the observations reported here provide the impetus for renewed consideration of Doushantuo fossils and their implications for red algal evolution.
Stratigraphic framework
The Neoproterozoic Era (1000–543 Myr) was a time of marked evolutionary innovation and dramatic environmental change. Various eukaryotic clades, including the red algae, green algae, stramenopiles, alveolates, and both lobose and filose amoebae, either appear for the first time in Neoproterozoic rocks or show evidence of increased morphological complexity and taxonomic diversity (Knoll, 1992
; Zhang et al., 1998
; Butterfield, 2000
; Porter and Knoll, 2000
; Xiao et al., 2002
). The Neoproterozoic Earth also experienced multiple global glaciations between about 750 Myr and 580 Myr (Hoffman et al., 1998
; Hoffman and Schrag, 2002
). Two of these events—the 
720 Myr Sturtian and the 600–660 Myr Marinoan glaciations—appear to have been global in extent, or nearly so. Additional ice ages may well be recorded in Neoproterozoic successions (Brasier et al., 2000
; Knoll, 2000
; Barfod et al., 2002
; Bowring et al., 2003
), although their geographic extent is poorly understood.
The Doushantuo Formation (Fig. 1) was deposited after one of these glaciations; Doushantuo rocks overlie glacial diamictites of the Nantuo Formation, probably the regional manifestation of Marinoan glaciation. Doushantuo rocks, in turn, are overlain by the Dengying Formation, a thick succession of carbonates that have yielded a succession of Ediacaran fossils (Sun, 1986
), Cloudina-like skeletal fossils (Chen et al., 1981
), and in its uppermost part, basal Cambrian small shelly fossils (Qian et al., 1979
). Therefore, the age of Doushantuo fossils is constrained stratigraphically by Nantuo glaciation and Ediacaran fossils. Correlations with radiometrically dated Neoproterozoic successions elsewhere indicate that the Doushantuo Formation must be between 600 and 550 Myr (Knoll and Xiao, 1999
), an estimate recently corroborated by a direct Pb–Pb date of 599 ± 4 Myr on fossiliferous Doushantuo phosphorites (Barfod et al., 2002
).
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; Steiner, 1994
; Ding et al., 1996
; Xiao et al., 2002
). At a number of localities in South China, shallow marine phosphorites are the predominant lithology of Doushantuo successions (Xiao and Knoll, 2000
; Zhou et al., 2002
). Of these, the phosphorites at Weng'an have become well known for their exquisite preservation of both animal embryos and multicellular algae (Xiao et al., 1998
). At Weng'an, the Doushantuo section is up to 40 m thick and contains two phosphate-rich units separated by a karsted surface. All algal fossils described in this paper come from the upper unit at Weng'an. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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).
Notes on systematic treatment
As will become clear in the subsequent discussion, three principal challenges attend the systematic investigation of phosphatized Doushantuo algae. First, it can be difficult to link observations made in random thin sections (two-dimensional) with those by SEM (three-dimensional). This problem is alleviated in the present study by thin sectioning isolated microfossils in controlled orientations. Second, it is difficult to reconstruct the life cycles of these fossils. Given that reproductive biology looms large in algal systematics and that heteromorphic alternation of generations is common among modern algae, this problem places potentially serious constraints on interpretation. Among other things, different life cycle stages of the same alga may bear distinct taxonomic names. It is perhaps beneficial to preserve the different names of suspected developmental stages, saving synonymy until various stages of the life cycle have been related unequivocally. This practice is common in paleobotany and is an approach adopted by early phycologists. Halicystis, for example, has been shown to be the gametophyte of Derbesia and Conchocelis an alternate stage of Porphyra. We follow our earlier practice (Zhang et al., 1998
) in treating all Doushantuo algae strictly as morphotypes. As will be clear from our discussion, however, we are aware that different morphological taxa may represent distinct developmental stages of a single species.
The third challenge is one faced in most investigations of early clade diversification: a clade's earliest records may be dominated by fossils that display some, but not all, features that collectively characterize younger members of the group. The recognition of crown groups (the minimal clade that includes all extant members of a group), stem groups (extinct members that have a closer phylogenetic relationship to the crown group than to any other crown groups), and total groups (crown group + stem group) greatly facilitates the phylogenetic interpretation of fossils (e.g., Budd and Jensen, 2000
). Nonetheless, as students of early eukaryotes (Javaux et al., 2003
), mollusks (Runnegar, 1996
), arthropods (Budd and Jensen, 2000
), and land plants (Edwards, 2000
) have recognized, the early fossil representatives of extant clades can be both tantalizingly familiar and frustratingly foreign, commonly at the same time.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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, Zhang and Yuan (1992)
, Zhang et al. (1998)
, and Yuan and Hofmann (1998)
. Zhang and Yuan (1992)
also tentatively compared the Doushantuo algal genus Thallophyca with extant Corallina. In this section, we present new observations that complement previous descriptions, with phylogenetic implications reserved for the section that follows. We begin with simple pseudoparenchymatous constructions with little-differentiated thalli and then proceed to more complex pseudoparenchymatous constructions characterized by medulla–cortex differentiation and, in some cases, specialized reproductive cells.
Simple pseudoparenchymatous construction: Wengania globosa (Figs. 2–5) and Wengania exquisita (Fig. 6)
Wengania is characterized by a circular thallus as observed in thin section and the absence of thallus differentiation into cortical and medullary layers. The three described species of Wengania are distinguished by thallus size, cell size, and cell organization. Thin sections of W. globosa thalli range from 70 to 750 µm in diameter (Figs. 2–5); the large range of observed sizes results, at least in part, from tangential sections through spherical thalli. The cuboidal cells (3–12 µm) of W. globosa form regular cell files that radiate outward and branch toward the thallus margin (Figs. 4–5). Wengania exquisita (Fig. 6) has a comparable thallus size but smaller cells (typically 2–4 µm). Its cell files are not so regularly arranged as those of W. globosa, so that its filamentous construction is less obvious. A newly described species, W. minuta, from Doushantuo cherts in the Yangtze Gorges area, is characterized by a small thallus size and intermediate cell sizes (44–200 µm and 3–8 µm in diameter, respectively), as well as the absence of well-organized cell files (Xiao, 2004
).
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). For the present, however, we retain Wengania species as distinctive morphotypes within the Doushamtuo assemblage.
Simple pseudoparenchymatous construction: Thallophycoides phloeatus (Fig. 7) and Gremiphyca corymbiata (Figs. 10–11)
Our new materials conform to previous descriptions and clarify the three-dimensional morphology of these two taxa. Thallophycoides phloeatus is spheroidal or lumpy in external morphology, lacks cell or thallus differentiation, and contains cells similar in size and structure to those of Wengania exquisita. Two specimens ascribed to T. phloeatus by Zhang et al. (1998
: Fig. 19.4–19.7) seem to have narrow invaginations that dissect the thalli into lobes. Gremiphyca corymbiata is characterized by a lobed, pseudoparenchymatous thallus that has no evidence of cellular differentiation. Internal cellular structure and cell size of G. corymbiata are somewhat similar to those of Wengania globosa, and their styles of thallus development may be similar as well. The lobes of G. corymbiata are more spheroidal than phylloid (Figs. 12–14). No holdfast structures have been observed in either of these two species. Nonetheless, both species were probably benthic, given their lobate thalli several hundred micrometers in size.
Complex pseudoparenchymatous construction: Thallophyca ramosa (Fig. 15) and Thallophyca corrugata (Figs. 16–19)
The genus Thallophyca is characterized by medulla–cortex thallus differentiation and clustered "cell islands" interpreted as reproductive cells (Zhang et al., 1998
). Clearly differentiated cortical layers have cells that are either smaller than (T. corrugata, arrow in Fig. 19) or oriented differently from (T. ramosa; Zhang et al., 1998
) medullary cells. In thin section, pseudoparenchyma is arrayed as upward diverging splays of filaments or cell fountains (Figs. 17, 22). Diverging filaments form fan-shaped lobes separated by deep invaginations (arrows in Figs. 15–16; see also Figs. 38, 39). Particularly striking are cylindrical, cell-lined invaginations that resemble conceptacles (Fig. 15).
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reconstructed the Weng'an alga Thallophyca ramosa as a foliose thallus. Most macerated specimens, however, are millimeter-scale spheroidal or irregular forms with swollen protuberances that range from columnar (Fig. 25) to spheroidal (Figs. 27–28) in shape. These isolated microfossils have well-preserved cell structures (Figs. 26) and sometimes evidence for cortex–medulla differentiation. Like the lobes seen in thin sections, protuberances are commonly dissected by deep invaginations (Figs. 25, 28). The protuberances tend to grow in one direction, suggesting that these algae were benthic.
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and Zhang and Yuan (1996)
as cystocarps with enclosed carpospores and carposporangia, structures that in living rhodophytes are associated with a triphasic life history. If so, P. incognata probably represents only one stage in a multiphasic life cycle. The vegetative thallus of P. incognata is pseudoparenchymatous, but the underlying filamentous structure is less conspicuous than in Thallophyca. Unlike Thallophyca, Paramecia thalli lack well-developed invaginations. Many macerated fossils are nodular in external morphology (Figs. 29, 34), but thin-section observations do not confirm the existence of cell differentiation and thallus compartmentalization (Figs. 31–33, 36). It is possible, but not at present demonstrated, that these fossils represent different developmental stages of P. incognata.
Summary of vegetative constructions
The most distinctive feature of phosphatized Doushantuo algae is their filamentous construction or "cell fountain" architecture (Zhang, 1989
). The pseudoparenchymatous architecture is most prominent in Thallophyca but is commonly also clear in Wengania, Paramecia, Thallophycoides, and Gremiphyca, despite variable attenuation from filament branching, cell reorganization related to differential cell expansion, possible cell fusion, and diagenesis. In several specimens, terminal cells are morphologically distinct from subtending cells of the same filament (Figs. 24, 41–42); these terminal cells may be meristematic apical cells responsible for filamentous extension and branching (arrowhead in Fig. 42).
Thallophyca and Paramecia display cell and thallus differentiation into an inner medulla and a thin peripheral cortex (Zhang, 1989
; Zhang and Yuan, 1992
; Zhang et al., 1998
). Although diagenesis can generate apparent zonation that mimics medulla-cortex differentiation (Figs. 8, 18), true thallus differentiation can be recognized by patterned variation in cell size and orientation (Figs. 19, 23). Cortical cells of Thallophyca ramosa are oriented tangentially to the thallus surface and perpendicularly to medullary cell rows (Zhang et al., 1998
). Cortical cells of T. corrugata are distinctly smaller than medullary cells (Fig. 19).
Possible reproductive structures
Cell islands and cavities (spheroidal gaps within algal thalli where no cellular structures are preserved) have been recognized in Thallophyca (Zhang, 1989
) and Paramecia (Zhang and Yuan, 1992
). These structures are not likely to be diagenetic artifacts because they are typically surrounded by tangentially oriented cells. In his original publication, Zhang (1989
, p. 118) hypothesized that the cavities "possibly represent conceptacle-like reproductive structures" and the cell islands may have served "a specific vegetative and reproductive function." Subsequently, the cell islands (e.g., Figs. 21, 50–51) were interpreted as cystocarps with carposporangia and carpospores (Zhang and Yuan, 1996
; Xiao et al., 1998
; Zhang et al., 1998
), structures borne on female gametophytes in living rhodophytes. Additionally, sorus-like structures with possible in-situ reproductive cells may also be reproductive structures (Fig. 44). The sorus-like structures are surrounded by tangential filaments. Within the sorus, larger, presumably reproductive cells are borne at terminal positions on vertical filaments.
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A carposporangium interpretation would be greatly strengthened by the discovery of gonimoblast filaments associated with connecting cells and auxiliary cells. However, the absence of these structures in cell islands does not necessarily falsify the carposporangium interpretation. First, the carpogonial branch and auxiliary cells are not easily recognizable in many red algae after the carposporophyte becomes mature. Second, gonimoblast filaments and auxiliary cells are derived and do not exist in the primitive florideophytes where gonimoblasts develop directly from fertilized carpogonia (Hommersand and Fredericq, 1990
). Third, even if they did exist in Doushantuo thalli, such structures might well be missed in randomly oriented thin sections.
Most florideophyte red algae are characterized by a separate, free-living tetrasporophyte phase. Is there evidence for tetraspores preserved in Doushantuo phosphorites? In our new material, we have found large (10–15 µm) monads, tetrads, and octads embedded in vegetative thalli composed of smaller cells (3–7 µm). Large spheroidal monads (Figs. 43, 48–49), some of which are demonstrably apical (Fig. 43), may be interpreted as tetrasporangial initials. Tetrads and octads (Fig. 46, 47) can be interpreted as tetraspores and octospores, respectively. Cruciately divided "tetrasporangia" appear to be subtended by two or more smaller cells (Fig. 47); these subtending cells are intriguingly similar to stalk cells supporting tetrasporangia in some florideophyte orders, for example, the Palmariales, Acrochaetiaceae, and Ceramiaceae (Guiry, 1974
, 1978
, 1990
; Hommersand and Fredericq, 1990
). Several uncertainties surround the tetrasporangia interpretation, however. First, tetrasporangia and polysporangia do not typically occur in the same red algal thallus, although there are rare exceptions, for example, in certain ceramialean species (Westbrook, 1930
; Maggs, 1988
). Second, these tetrads/octads are surrounded by a thick, multi-laminated envelope (Fig. 47) that resembles cyanobacterial sheaths. Third, a mechanism for tetrad/octad discharge is not obvious, raising the possibility that these cells might have continued to divide in situ, eventually forming berry-like cell islands (cf. Figs. 20–21, 50–51). Fourth, the tiered arrangement of the octads (Fig. 46) seems to be unusual in florideophyte polysporangia or, for that matter, phaeophyte plurilocules. Considering these uncertainties, these tetrads/octads can be alternatively interpreted as endophytic cyanobacterial colonies or commensal algae that grew intimately within the smaller-celled thalli.
Cell wall microstructures
Under light microscopy, cell walls are usually preserved as a thin, dark trace coated by clear phosphatic minerals on both sides (Figs. 11, 52). In less well-preserved specimens, this dark trace can be lost and the space between cellular internal molds filled with diagenetic phosphate or carbonate (see Boyce et al., 2001
, for examples of comparable preservation in petrified wood). Under SEM, the cell walls of Doushantuo algae look very similar to the calcified walls of some coralline red algae (Johansen, 1981
; Woelkerling, 1988
), but mineral precipitation on Doushantuo cell walls occurred during early diagenesis and not in life (Xiao and Knoll, 2000
).
In many Doushantuo algae, cell walls are interrupted by transverse gaps that are about 1–8 µm wide and occupy one-eighth to one-half of the shared walls between neighboring cells (arrows in Fig. 52). These gaps may represent cell fusion, although a diagenetic origin cannot be completely ruled out. If the presence of cell fusion can be confirmed, it would provide important evidence for the phylogenetic interpretation of these algal fossils, because cell fusion is a common feature of red algal anatomy, particularly in the Corallinales (Johansen, 1981
).
At higher magnification with light microscopy, rare transverse canals (<0.5 µm wide) are present on cell walls, linking neighboring cells. There is an intriguing possibility that these canals may represent pit connections. However, we have not confirmed their existence under SEM; thus, it is currently impossible to compare these canal structures with SEM observations of red algal pit connections (Pueschel, 1988
). Therefore, the presence of cell fusion and pit connection structures in Doushantuo algae remains speculative.
Biocalcification
Although much smaller, the thalli of Gremiphyca, Thallophycoides, Thallophyca, Paramecia, and Wengania resemble in external morphology to Cenozoic rhodoliths—centimeter-sized, ellipsoidal, spheroidal, or discoidal grains constructed principally by crustose corallinaleans (Bosence, 1983a
, b
; Hottinger, 1983
; Gischler and Pisera, 1999
). Indeed, Zhou and Xue (1999)
interpreted some phosphatized Doushantuo algae as rhodolith corallines. As discussed in the next section, some Doushantuo algae display broadly coralline features and may be stem group corallinaleans. They are, however, clearly distinct from crown group corallines (the Corallinaceae and Sporolithaceae). A key difference is that the Doushantuo algae were not calcified in life, as indicated by taphonomic evidence (Xiao and Knoll, 2000
). Furthermore, there is no evidence that the Doushantuo algae were crustose thalli superimposed on each other, as many rodoliths are.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
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) have evolved three-dimensional multicellular thalli, our search focuses on these algal groups.
General considerations
Apical growth and filamentous/pseudoparenchymatous construction are characteristic of such Doushantuo algae as Wengania, Thallophycoides, Gremiphyca, Thallophyca, and Paramecia. Apical growth arose independently in florideophyte red algae, charophyte green algae, and various brown algae. Charophytes are excluded from further discussion because their nodal-internodal construction and whorled lateral branches distinguish them unambiguously from the Doushantuo thalli. In some brown algae, such as Dictyota and Fucus, one or several apical cells, together with intercalary cells, are responsible for algal growth and bifurcation. However, these brown algae have true parenchymatous thallus construction, making them inappropriate analogs to Doushantuo thalli. The thallus of another brown alga, Ralfsia, is constructed by meristematic apical cells and composed of pseudoparenchymatous cell rows (Fletcher, 1978
), in a way very similar to the Doushantuo thallus Thallophyca. The perithallus-hypothallus differentiation and crustose habit of Ralfsia thalli, however, distinguish this genus from Thallophyca. More importantly, unilocular or plurilocular sporangia, characteristic of many brown algae, have not been found in Thallophyca or any other Doushantuo thalli. Therefore, the likelihood of a phaeophyte affinity for the Doushantuo algae appears to be small.
Better morphological analogs for the Doushantuo fossils are found in the red algae, particularly when possible reproductive and cell fusion structures are considered. Phycologists have traditionally recognized two classes within the rhodophytes: the relatively undifferentiated Bangiophyceae and the more complex (and far more diverse) Florideophyceae. Molecular phylogenies show that the monophyletic florideophytes are nested within the paraphyletic bangiophytes, forming a sister group to the Bangiales (Oliveira and Bhattacharya, 2000
; Müller et al., 2001
). Most bangiophytes species are unicellular, and those that do form true filaments (Rhodochaete, bangialean conchocelis phase) have open branching. Substantial pseudoparenchymas are not formed by any bangiophytes. Bangialean gametophytes may develop a rudimentary parenchyma, but these thalli have little anatomical differentiation.
The modes of thallus development in the Florideophyceae are more diverse, but apical divisions and openly filamentous or pseudoparenchymatous construction are both universally present in the clade (Coomans and Hommersand, 1990
; Waaland, 1990
). Despite the underlying uniformity of filamentous construction, morphologies range widely because the filaments show varying degrees and patterns of branching, lateral adherence, compaction, differentiation of determinate and indeterminate filaments, and size differentiation of cells within a filament. The pseudoparenchymatous nature of thalli can obscure even fundamental differences of construction, such as whether the thallus grew from a single (uniaxial) or many indeterminate apical cells (multiaxial). Nonetheless, the pseudoparenchymatous constructions of the Doushantuo fossils suggest that they are much more likely to be florideophytes than bangiophytes.
Assigning these fossils to any particular florideophyte order is, however, difficult for several reasons. First, classification of the Florideophyceae at the ordinal level has been in a state of flux since Kylin's work (Kylin, 1956
), although it has been stabilized to some degree in recent years in the wake of phylogenetic analyses using both morphological and molecular data (Pueschel and Cole, 1982
; Gabrielson and Garbary, 1987
; Freshwater et al., 1994
; Ragan et al., 1994
; Saunders and Kraft, 1997
; Harper and Saunders, 2001b
; Müller et al., 2002
). Second, the independent evolution of similar gross morphology and pseudoparenchymatous anatomy by divergent florideophytes and the significantly different levels of anatomical and morphological complexity found within a single life history have limited the value of these vegetative features in ordinal systematics and phylogenetic considerations.
Reproductive morphology, particularly carpogonial branches and post-fertilization development, may provide the principal criteria for ordinal systematics of the florideophytes. However, basing a taxonomic system on complexity of reproductive morphology has the inevitable result of artificially grouping reproductively simple taxa in an assemblage of "have-nots." The diversity of these reproductively simple florideophytes has been revealed by their molecular systematics (Freshwater et al., 1994
; Ragan et al., 1994
; Saunders and Kraft, 1997
; Harper and Saunders, 2001b
; Müller et al., 2002
) and analysis of their ultrastructural characters, particularly pit plugs (Pueschel and Cole, 1982
; Pueschel, 1989
). Because of their antiquity, the Doushantuo red algae are expected to be among the reproductively simple (and, therefore, harder to discriminate) types. In the following paragraphs, we briefly summarize the morphological features of the early diverging florideophyte clades. The clades are considered in order of divergence, as indicated by rDNA sequence data (Fig. 53A).
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Corallinales/Rhodogorgonales
Members of the Corallinales have a variety of anatomical specializations, and some of these are unique to the group: the cells making up the thallus surface are mostly specialized, nondividing epithallial cells, and the thallus thickens by the activity of intercalary meristematic cells (Johansen, 1981
). A variety of other distinctive features present in corallines are neither universal within nor unique to the order. These features include extensive direct fusion or secondary pit connections between cells, an articulated structure of alternating calcified and uncalcified segments, and reproductive structures borne in conceptacles. However, the most conspicuous feature of living corallines is the presence of pervasively calcified cell walls, and perhaps many of the distinctive features of corallines are related to pervasive calcification. Molecular systematics indicates that the Rhodogorgonales is closely associated with the Corallinales (Saunders and Bailey, 1997
; Harvey et al., 2002
). All members of both orders precipitate calcite, but mineralization in the Rhodogorgonales consists of individual crystals deposited in the mucilagenous matrix/wall that surrounds only specialized calciferous cells (Pueschel et al., 1992
). The differences in anatomy and the mode of calcification between the Rhodogorgonales and Corallinales are so great as to suggest that these two lineages may have evolved calcification independently.
Ahnfeltiales
Gametophytes of Ahnfeltia are erect, terete, and dichotomously branched. They have a compact pseudoparenchyma and anatomical differentiation into medulla and cortex. However, the crustose tetrasporophyte phase shows little anatomical differentiation. Vertical filaments are strongly coherent and are composed of cells of uniform size, except for those that have undergone direct cell fusion. Reproductive morphology is simple (Maggs and Pueschel, 1989
).
Nemaliales/Acrochaetiales/Palmariales/Batrachospermales complex
The Acrochaetiales are generally small, structurally simple, and consist of openly branched thalli. The Palmariales, by contrast, can consist of hollow, pseudoparenchymatous tubular thalli, or blades with a large-celled medullary zone. The underlying filamentous construction of the thallus is not easily discerned. Most members of the Nemaliales retain a more obviously filamentous construction, but some have a coherent, pseudoparenchymatous cortex that shows little outward sign of being filamentous. Calcification is common in some nemalialean taxa, but the mineral form is aragonite and deposition involves fewer specializations and less anatomical integration than is seen in the calcitic clade.
The remaining lineage contains the great majority of florideophyte orders, including the Gigartinales, Ceramiales, Rhodymeniales, and Gelidiales. The Ceramiales, which contain many openly branched filamentous species, appear to branch first in some small subunit (SSU) trees (Saunders and Kraft, 1997
; Müller et al., 2002
), whereas a species of Peyssonnelia is basal in the large subunit (LSU) trees and other SSU trees (Harper and Saunders, 2001b
). Peyssonnelia is a crustose genus with many species depositing aragonite.
Simple pseudoparenchymatous construction
The simple pseudoparenchymatous constructions of such Doushantuo fossils as Wengania, Gremiphyca, and Thallophycoides are comparable to the little differentiated thalli of the Hildenbrandiales and Ahnfeltiales. However, as has already been stressed earlier, ordinal assignment based on morphological simplicity, rather than distinct features (such as thallus differentiation and reproductive structures), can be problematic. It is perhaps safer to consider these Doushantuo algae as lineages that branched near the base of the florideophyte tree, before the divergence of more complex orders. They could be stem group florideophytes, stem groups to one of the earlier branching crown group clades, or simple members of early branching crown groups.
Complex pseudoparenchymatous construction
Thallophyca and Paramecia display more complex thalli and possible reproductive structures, including conceptacles/sori. Conceptacles are present and probably independently evolved in two early lineages, the Hildenbrandiales and Corallinales (Pueschel, 1982
). The conspicuous filamentous construction and moderate degrees of thallus differentiation in Thallophyca and Paramecia compare more closely to the Corallinales (particularly some Paleozoic fossils allied to the corallinaleans) than to the Hildenbrandiales. We therefore argue that the complex pseudoparenchymatous thalli in the Doushantuo Formation represent stem group corallinaleans.
The order Corallinales, which is probably a monophyletic group, consists primarily of marine calcareous rhodophytes (Johansen, 1981
; Woelkerling, 1988
; Bailey and Chapman, 1998
). The Corallinales clade branched near the base of the florideophyte phylogenetic tree (Ragan et al., 1994
), and the crown group Corallinales includes two living families, Corallinaceae and Sporolithaceae (Verheij, 1993
; Townsend et al., 1995
), with the latter considered a basal clade sister to all subfamilies of the Corallinaceae (Bailey and Chapman, 1998
). The widely cited fossil genus Archaeolithothamnium is regarded as a junior synonym of Sporolithon, the eponymous genus of the Sporolithaceae (Moussavian and Kuss, 1990
; Verheij, 1993
). Vegetative thalli of the Corallinales have various habits (encrusting, foliose, lumpy, nodular, or arborescent; nongeniculate or geniculate; attached or free-lying). Both Corallinaceae and Sporolithaceae are characterized by thallus differentiation into a hypothallus composed of prostrate filaments, a perithallus of erect filaments, and a thin epithallus made up of one or a few cell layers. Large, hair-bearing trichocytes are present in Corallinaceae. Cell fusion is also common in corallinalean algae. Reproductive cells are housed in sori (with plugs, Sporolithaceae) or conceptacles (with one or more openings, both Sporolithaceae and Corallinaceae) that typically occur in layers. Tetraspores are either zonate (Corallinaceae) or cruciate (Sporolithaceae). In Sporolithaceae, a tetrasporangial initial cell divides unequally into a small basal stalk cell and a larger tetrasporocyte from which tetraspores are generated.
Doushantuo pseudoparenchymatous thalli, particularly Thallophyca and Paramecia, have broad similarities to the Corallinales. Their thalli are lumpy, nodular, or spheroidal. The pseudoparenchymatous construction, particularly in Thallophyca (Figs. 16–19, 22), is strikingly similar to the Corallinales. Thalli of Thallophyca do differentiate into cortical and medullary layers, although no structures interpretable as epithallus, hypothallus, or perithallus have been observed. The outwardly divergent splays of filaments (or cell fountain structures) are very similar to some corallinalean algae. The possible presence of cell fusion, carposporangia, tetrasporangia (cruciate and stalked), and sori in Doushantuo thalli would also strengthen a corallinalean comparison. Interestingly, cruciate tetraspores, stalk cells, and sori are all features present in the primitive family Sporolithaceae (Verheij, 1993
; Townsend et al., 1995
; Bailey and Chapman, 1998
).
Despite their broad similarities, the Doushantuo thalli are distinctively different from living corallinaleans. The Doushantuo thalli are typically millimeters rather than centimeters in size—much smaller than living corallineans. They developed no equivalents of the hypothallus, perithallus, or epithallus. Their transverse cell walls do not always align across different filaments. And their reproductive sori do not line up in layers. Although hypothallus–perithallus differentiation, laterally aligned cells, and layered sori are not universally present in all living corallines, the Doushantuo thalli do differ in an important aspect from the crown group corallines—biocalcification. More interestingly, derived corallinacean features, including zonate tetrasporangia, trichocytes, and true conceptacles (with openings and paraphyses), are entirely absent in the Doushantuo thalli. This prompts us to consider the idea that the Doushantuo pseudoparenchymatous thalli may have branched before the Corallinaceae–Sporolithaceae divergence; in other words, they may be stem group corallinaleans.
Morphologically modern coralline algae radiated during the Cretaceous and Tertiary periods (Aguirre et al., 2000
). Because of the immense stratigraphic gap between Doushantuo stem groups and Mesozoic crown groups, we should search connecting fossils in Paleozoic rocks. Several taxa of possible stem group corallinaleans have been described from Paleozoic carbonates. Most were placed in the family Solenoporaceae (Wray, 1977a
, b
; Johansen, 1981
), but recent research shows that many (including the type species of Solenopora, S. spongioides) may not be red algae at all (Brooke and Riding, 1998
; Riding, 2004
). Several Early Paleozoic fossils, however, do appear to be calcified corallines, including the Ordovician taxa Arenigiphyllum crustosum, Petrophyton kiaeri, and "Solenopora" richmondensis, and the Silurian Graticula gotlandica (Blackwell et al., 1982
; Brooke and Riding, 1998
, 2000
; Riding et al., 1998
). Indeed, G. gotlandica preserves features of anatomy and reproductive biology that specifically ally it to younger coralline algae (Brooke and Riding, 1998
, 2000
; Riding et al., 1998
). In comparison to the Doushantuo fossils Thallophyca and Paramecia, these Paleozoic thalli display a number of features that place them phylogenetically closer to crown group corallinaleans. These include biocalcification, hypothallus–perithallus differentiation, aligned cross partitions, calcified sporangial compartments, and trichocytes.
The morphological and stratigraphic gaps are further bridged by late Paleozoic "ancestral corallines" such as Archaeolithophyllum (Johnson, 1956
; Wray, 1977a
, b
; Brooke and Riding, 1998
). Archaeolithophyllum displays an array of features, such as conceptacle-like structures embedded in the perithallus, that place it even closer to crown group corallines. The broad picture, then, suggests that the Mesozoic radiation of crown group corallinaleans was preceded by soft (uncalcified) stem groups such as Thallophyca and Paramecia in the Neoproterozoic, followed by calcified stem groups such as Arenigiphyllum, Petrophyton, Graticula, and Archaeolithophyllum in the Paleozoic (Fig. 53B). This evolutionary scheme is consistent with both the stratigraphic occurrences of these algal fossils and the long-held notion that the Paleozoic "Solenoporaceae" and "ancestral corallines" represent evolutionary antecedents of the crown group Corallinales (Wray, 1977a
, b
; Johansen, 1981
; Brooke and Riding, 1998
). The fossil record of other early diverging florideophyte clades, such as the Hildenbrandiales, is so far unknown because the red algal fossil record remains sketchy and strongly biased toward calcareous taxa.
One implication of this view is that bangialean–florideophyte divergence must have taken place in the Neoproterozoic or earlier. Indeed, the earliest known red algal fossil, Bangiomorpha pubescens, from ca. 1.2 x 109-year-old rocks in Arctic Canada, compares closely with living Bangia and has been interpreted as a member of the Bangiales (Butterfield et al., 1990
; Butterfield, 2000
). Late Neoproterozoic diversification of macroscopic florideophytes and green algae, recorded by compression and trace fossils as well as petrifactions (Xiao et al., 2002
; Knoll and Xiao, 2003
), may reflect environmental as well as genetic changes (e.g., Anbar and Knoll, 2002
).
|
CONCLUSIONS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
Thallophyca and Paramecia, characterized by pseudoparenchymatous thallus, apical growth, thallus differentiation, and possible specialized reproductive structures, can be broadly compared with the Corallinales (Zhang and Yuan, 1992
; Zhang et al., 1998
), but many derived characters (e.g., biocalcification) of the Sporolithaceae and Corallinaceae were not present in the Doushantuo algae. Thallophyca and Paramecia are therefore considered stem group corallinaleans. Along with calcified "ancestral corallines" in the Paleozoic, such as Arenigiphyllum, Petrophyton, Graticula, and Archaeolithophyllum, they appear to represent lower rungs on an evolutionary ladder that led, through time, to the crown group Corallinales.
In closing, we reiterate that while the phylogenetic hypotheses discussed here are reasonable, significant uncertainties remain. In particular, the interpretation of embedded cell clusters as tetrasporangia and carposporangia in Doushantuo thalli remains problematic, although such reproductive structures might be expected if these fossils are florideophytes with a triphasic life cycle. Continuing discovery and analysis, including the use of MicroCT techniques to resolve three-dimensional structures embedded in thalli, promise to refine our ideas about the nature of Doushantuo algae.
|
FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
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