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Taxonomy, slime molds, and the questions we ask

     Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas 72701

James C. Cavender

     Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

Taxonomic treatments often influence the way we both ask and attempt to answer certain biological questions. The classical taxonomy of the dictyostelid cellular slime molds (Dictyosteliales) involves a convenient set of categories that were developed independent of phylogeny. In order to test whether the characters supporting the classical taxonomy hold any phylogenetic signal, we subjected 19 described taxa belonging to two families (Acytosteliaceae and Dictyosteliaceae) and three genera (Acytostelium, Dictyostelium, and Polysphondylium) to rooted cladistic analyses using PAUP* v 4.0b4a. Neither family nor any of the three genera were found to represent monophyletic groups. These results confirm that the classical taxonomy used to delineate families and genera within these slime molds carries very little phylogenetic signal. Taxonomic character sets should be scrutinized phylogenetically in order to determine what information they provide about the relatedness of taxa within a group. Because taxonomy often drives the nature of biological inquiry, caution should be exercised when drawing conclusions regarding the evolution of developmental systems in Dictyostelium.

Key words: Acytostelium, Dictyostelium, Eumycetozoa, Phylogeny, Polysphondylium

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
A phylogeny is a scientific hypothesis. A taxonomy by itself is not. Yet we often treat taxonomies as hypotheses, and the questions we pose regarding phylogenetic relatedness are often driven by the insinuations taken from the underlying taxonomy. The rules of both botanical and zoological nomenclature emphasize stability (Mayr and Ashlock 1991, Greuter et al 2000). With the classical identification, naming, and subsequent cataloging of new species, evolutionary theory has historically taken a secondary role to the traditional (and intuitive) view that similarity of form (whether macroscopic, microscopic, or molecular) should indicate relatedness between taxa. Morphological, physiological, behavioral, and genetic characteristics are certainly important in the development of a taxonomic system. Once in place, however, a taxonomic system intrinsically drives the nature of biological inquiry, typically by inspiring assumptions about the evolutionary processes that contribute to the diversity of form.

The classical taxonomic grouping of Oomycota with fungi, for example, encouraged the assumption that filamentous growth and absorptive nutrition were synapomorphies unifying them with the Fungi. We now know that oomycetes are phylogenetically allied with the heterokont algae (Barr 1992), a lineage quite removed from the Opisthokonts [Fungi and Animals (Cavalier-Smith 1998)]. This phylogenetic realization verifies convergence of a key taxonomic character–filamentous hyphae—and leads to the awareness that traditional taxonomy has impeded formulation of the most fundamental and pertinent questions regarding hyphal origins in all groups of mycelial organisms (e.g., how many times have hyphae originated?).

Similarly, the aggregation of single amoebae into a multi-celled fruiting body was an important taxonomic character that unified the acrasids (sensu Olive 1975) and dictyostelid cellular slime molds into a larger Class Acrasiomycetes (Raper 1984). Olive's (1975) observations leading to studies by Page and Blanton (1985), and Roger et al (1996) have demonstrated that the acrasids are members of the Heterolobosea, a group phylogenetically distant from the Eumycetozoans. Differences in morphology have turned out to be more important than superficial similarities of aggregation, and again, convergence has been recognized in what was traditionally viewed as a unique evolutionary event.

Taxonomic treatments influence the way we form our inquiries, and we often fail to ask the right questions about the evolutionary mechanisms involved if, for instance, convergence of characters is never considered. This trap is well camouflaged, owing first to modern taxonomy's presumed acceptance of an evolutionary worldview, and second to the history of nomenclature in each group of related organisms. Biologists must be mindful that our ideas about how characters evolve can be highly influenced by taxonomy.

Subclass Dictyosteliidae, Order Dictyosteliales is clearly a monophyletic assemblage (Table I) within the Eumycetozoa, a natural group that includes the protostelid, dictyostelid, and myxogastrid slime molds (Olive 1975, Dykstra 1977, Drouin et al 1995, Spiegel et al 1995, Keeling and Doolittle 1996, Baldauf and Doolittle 1997, Baldauf 1999). The Dictyosteliales have traditionally been divided into two families: the Acytosteliaceae (which includes Acytostelium), with an acellular, hollow stalk, and the Dictyosteliaceae (which includes Dictyostelium and Polysphondylium), which have a cellular stalk (Olive 1975, Raper 1984). Oskar Brefeld (1869) was the first to isolate and describe a dictyostelid, Dictyostelium mucoroides, whose generic name was chosen based on the net-like appearance of the fruiting body's stalk cells (Raper 1984). Members of Dictyostelium possess relatively large fruiting bodies that are typically unbranched or irregularly branched (Fig. 1a). Brefeld later (1884) described a second species, Polysphondylium violaceum, complete with a new generic designation based on the regularly-whorled branches of the fruiting body's cellular stalk (Fig. 1b). These two genera were included in the family Dictyosteliaceae. Acytostelium leptosomum, described by Raper in 1956, and later characterized fully by Raper and Quinlan (1958), possessed tiny, delicate fruiting bodies with acellular hollow stalks (Fig. 1c), and was deemed unique enough to be assigned to a third genus in its own, new family Acytosteliaceae.

View larger version (10K): [in this window] [in a new window]    FIG. 1. a. Dictyostelium mucoroides, b. Polysphondylium violaceum, c. Acytostelium leptosomum. Bar = 1 mm

View larger version (9K): [in this window] [in a new window]    FIG. 2. Proposed evolutionary relationships among the Eumycetozoa (modified from Olive 1975).

Outgroup selection is obviously an important matter, and for examining relationships within the Dictyosteliales, the use of a Eumycetozoan sister taxon is most appropriate. Olive and Stoianovitch (1960) hypothesized a relationship between the protostelid Protostelium mycophaga and the dictyostelid genus Acytostelium based on the two groups' very similar non-flagellated amoebae and acellular fruiting body stalks. Molecular work has supported a close relationship between Protostelium and dictyostelids (Dutta and Mandel 1972, Spiegel et al 1995), as well as between the protostelid Planoprotostelium (a close relative to Protostelium (Spiegel 1990)) and Dictyostelium (Baldauf and Doolittle 1997). Spiegel et al (1979) suggested that the similarities during culmination among stalk tube-synthesizing cells of dictyostelids and protostelids indicated a shared evolutionary history as well. These studies have lent considerable support to Olive's (1975) hypothesis that a protostelid-like ancestor gave rise to Dictyostelids (Fig. 2).

In this paper, we use formal phylogenetic analysis to investigate whether the traditional taxonomic characters impart any information about the evolutionary relatedness of 19 members of the Dictyosteliales in order to determine if those characters support the current classification of two families and three genera. We test two hyphotheses that are consistent with the current taxonomy: (i) acellular stalk is a plesiomorphic character state, while cellular stalk is a synapomorphy that defines the family Dictyosteliaceae; (ii) evenly-spaced whorled branching is a synapomorphy that defines the genus Polysphondylium. We also discuss the influence our results may have on the formulation of questions about the evolution of key characters defining the two families and three genera of the group.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
A data matrix containing 18 characters was constructed for 1 protostelid outgroup (Protostelium mycophaga) and 19 ingroup taxa (Table II). Characters were drawn from the taxonomic literature and chosen according to their universality among members of the Dictyosteliales. Character coding was made according to the taxonomic works of Raper (1984), Hagiwara (1989), Olive (1975), and original published species descriptions. The 19 dictyostelid taxa were chosen to cover the range of morphological and developmental diversity found in the roughly 65 described species (Swanson et al 1999). The final matrix was analyzed using PAUP* v 4.0b5 for Macintosh (Swofford 1999) applying branch and bound methods for maximum parsimony, with characters defined as unordered and with equal weights. Unrooted strict and 80% majority rule consensus trees were constructed.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

View larger version (12K): [in this window] [in a new window]    FIG. 3. A. Strict consensus of 36 most parsimonious trees. B. 80% Majority rule consensus of 36 most parsimonious trees; numbers indicate percent of trees that support the topology. (see Table II, footnote ‘a’ for species abbreviations)

View larger version (13K): [in this window] [in a new window]   FIG. 3. Continued.

Using strict consensus, there is no support for a single clade that contains all of Polysphondylium, although the 80% consensus tree lends some support for a monophyletic group containing the white-spored species of Polysphondylium (Fig. 3b).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The trees generated from the present character set do not support the classical arrangement of families into Acytosteliaceae and Dictyosteliaceae, nor do they support a monophyletic genus, Polysphondylium.

The current taxonomy of dictyostelids implies that cellular stalk arose once, and is a synapomorphy of the Dictyosteliaceae, and that whorled branching arose once, and is a synapomorphy of the genus Polysphondylium. These have been unquestioned assumptions in all published speculation on the phylogeny of the dictyostelids. Four possible phylogenetic arrangements are consistent with the hypotheses implied by the current taxonomy ( Fig. 4a–d ). At one extreme (Fig. 4a), all three genera and both families are monophyletic. At the other extreme, the only monophyletic genus is Polysphondylium and the only monophyletic family is the Dictyosteliaceae (Fig. 4d). In one intermediate tree, Acytostelium and Polysphondylium are monophyletic, and both families are monophyletic (Fig. 4b). In the other intermediate tree, the Acytosteliaceae and Acytostelium are paraphyletic, the Dictyosteliaceae is monophyletic, and within the Dictyosteliaceae, both Dictyostelium and Polysphondylium are monophyletic (Fig. 4c). None of these tree topologies is consistent with those generated in the current study (Fig. 3a, b). Therefore, the phylogenetic hypotheses implicit in the current taxonomy must be rejected as a natural system unless additional support is provided by other data sets.

View larger version (15K): [in this window] [in a new window]    FIG. 4. A–D. Four phylogenetic arrangements consistent with the current taxonomy. A, B, and C represent the origins of streaming aggregation, cellular stalks, and whorled branching respectively

View larger version (16K): [in this window] [in a new window]   FIG. 4. Continued.

When the characters drawn from the traditional taxonomy are used for phylogenetic analysis, Acytostelium is paraphyletic, found in several clades basal to the clade that includes the bulk of Dicytostelium and Polysphondylium (Fig. 3a). Therefore, it is likely that acellular stalk, the character state that defines Acytostelium, is indeed plesiomorphic for some of the Acytostelia. The basal position of Dictyostelium lacteum, however, lends support to the idea that cellular stalk, the character state that defines the Dictyosteliaceae has arisen more than once. Alternatively, the cellular stalk may have arisen only once, just basal to the clade that contains D. lacteum, and a character state reversal in the lineage leading to A. ellipticum is the basis for this species' secondarily acellular stalk. This being said, because of the implications of the classical taxonomy, the question of how cellular stalks evolved has not been adequately addressed. By refuting the hypothesis that cellular stalks have evolved only once, a wide range of evolutionary and developmental questions become apparent, questions that have not been posed due to restraints implicit in the taxonomy.

The position of D. lacteum is not entirely surprising. Robertson and Cohen (1972) speculated a "primitive" position for this species in the genus based on the relative complexity of developmental control systems and morphogenesis. Various other investigators have pointed out the close resemblance of this species to members of Acytostelium (Bonner 1967, Olive 1975). In fact, Bonner and Dodd (1962) reported that the stalks of D. lacteum contained lower cellular as well as upper acellular portions.

Using all of the taxonomic characters for phylogenetic analysis, there is no support for a monophyletic Polysphondylium. Members of the genus Polysphondylium emerge from two separate relatively apical unresolved polytomies (Fig. 3a). This analysis supports the notion that regularly spaced, whorled branching, the character state that defines Polysphondylium, is homoplasic, having likely arisen more than once (although it is possible that some members of Dictyostelium could be secondarily whorl-less). Debate about the significance of whorled branching has endured since Van Tieghem (1884) first questioned its suitability for defining a new genus (Potts 1902, Olive 1902, Rai and Tewari 1963, Raper 1984). Cox et al (1988) have suggested a relatively simple model for whorl formation that involves the interplay between chemotactic movement of cells forward, and cohesion of cells to each other. The spatial patterns of whorl formation are genetically controlled (Spiegel and Cox 1980, Cox et al 1988), but the spacing of whorls in nature may be induced or constrained by the specific micro-spatial environment that the organism occupies. Spore dissemination is the key driving force to extending the spore mass upward and/or outward, regardless of structural mechanism, and successful dispersal in nature often depends on the extension of the spore masses into appropriately large spaces in the soil. A whorling dictyostelid would therefore be able to place spores in many interstitial spaces that could be traversed by invertebrate vectors. Species with a single sorus of spores would only extend into one space. Selective pressure would likely favor "opportunistic whorling" in these instances, wherein the effectiveness of spore dispersal is maximized, without unessential cell differentiation in the migrating slug.

Polysphondylium violaceum, the type species of the genus (Brefeld 1884), emerges from within a terminal clade that includes other pigmented dictyostelids. This result is not altogether remarkable, as P. violaceum differs from the unpigmented members of Polysphondylium in several other respects, including the presence of consolidated polar granules in the spores and a marked phototropism of the migrating slug. If Brefeld had defined the genus Polysphondylium based on P. violaceum's unique sori and stalk pigmentation, rather than on its stalk's regular whorled branching pattern, perhaps the range and scope of evolutionary questions raised about the group would be quite different. Speculation aside, based on our data set, we reject the hypothesis that Polysphondylium is monophyletic and that whorled branching has arisen only once.

Following the proposals of Graybeal (1998), additional taxa and characters were added to and removed from the data matrix in an attempt to support one of the hypothetical trees consistent with the classical taxonomy of the group. Only slight differences in topologies were generated, and these each remained inconsistent with the classical taxonomy. No clades were found that exclusively contained all members of either Acytosteliaceae or Dictyosteliaceae. Dictyostelium lacteum never grouped with the cellular-stalked dictyostelids. Polysphondylium could be made monophyletic with the removal of several characters from the data matrix (i.e., growth habit, pigmentation, and base/tip shape), but this made the a priori assumption that whorled branching was a unifying synapomorphy. When whorled branching was removed from the data matrix, no combination of the remaining characters could hold Polysphondylium together in a single clade. We conclude that it is unlikely that adding more developmental and/or morphological characters will generate cladograms with topologies consistent with the classical taxonomy, although perhaps data from molecular analyses may generate trees with different topologies.

Clearly, a phylogenetic analysis using taxonomically valuable characters does not support a classification that is consistent with the current taxonomy. Further, equation of the classical taxonomy with a phylogenetic hypothesis has prevented us from asking the most appropriate evolutionary and developmental questions. For example, what evolutionary processes could lead to differences in stalk cellularity and/or regular whorled branching? Are the developmental genetics for stalk cellularity in D. lacteum the same for other members of Dictyostelium? Are the developmental genetics for whorled branching the same in P. violaceum and P. pallidum? In highlighting the poor understanding we have of dictyostelid evolution, we also emphasize our limited understanding of the evolution of many intricate processes that have made these slime molds (particularly Dictyostelium discoideum) such attractive and powerful model systems for the study of basic cell and developmental biology. If D. discoideum is a model system, then we need to know how it fits into the phylogenetic milieu of the dictyostelids in order to fully understand the implications of its biology. The evolution of cellular stalks, delays in stalk synthesis, and the "altruistic" nature of stalk formation for example, are significant events in slime mold evolution. We must be careful to consider the question of what is strictly a D. discoideum characteristic, what is a Dictyostelium characteristic, and what is a general biological characteristic. We should not rely on the prevailing taxonomy to make those decisions for us. It would benefit us to evaluate how generally applicable these characteristics are within the group before we can speculate on how generally applicable they are outside the group.

We are not presenting these phylogenetic hypotheses as a final answer, nor are we suggesting taxonomic revision. Certainly, molecular work may result in trees with different topologies, perhaps even a tree supporting one of the hypotheses implied by the current taxonomy. Our point is, whatever taxonomic character set is adopted for a particular group of organisms should be phylogenetically tested so as not to preclude a wider range of potential hypotheses from being tested, and a more pertinent range of questions from being posed. Each time new characters are introduced, they too should be processed phylogenetically to determine what, if anything, they indicate about the evolutionary relationships within the group. In this time of integration of biological thought and synthesis of a new biological paradigm, it is important to recognize that as much as taxonomic criteria aid in the development of phylogenetic hypotheses, so obviously should phylogenetics guide accurate taxonomy.

	ACKNOWLEDGMENTS

 
The authors wish to thank Dr. J. M Turbeville, Department of Biology, Virginia Commonwealth University, for assistance with PAUP* and for helpful suggestions concerning our results.

	FOOTNOTES

 
¹ Corresponding author, arswans{at}uark.edu

Accepted for publication May 22, 2002.

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