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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

[ref. ID; 4978 (F.J.R. 'Max' Talor, 2003)]

The dualistic Plant-Animal view had its roots in Aristotle and his teacher Plato, in the Academy in Athens almost 2500 years ago (ca. 360 BC). Two living supergroups were formalized in 1735 by Carl von Linne in his monumental "Systema Nature" as the Kingdoms Plantae and Animalia, into which all organisms were placed. By the 12th, and last, edition (Linnaeus 1766), he had added a third kingdom of the natural world, Lapides (for 'rocks'; solid bodied, not living, not 'sentient', i.e. not having 'senses', a trait shared with plants in his scheme). This division of the living world was reflected in the disciplines of Botany and Zoology, housed in their own separate academic Departments for more than 250 years. Beginning in the mid 20th century, accompanying growing realization that plant and animal cells were fundamentally very similar in biochemistry, structure and genetic systems, a more common biological approach began. This was reinforced unequivocally by the 1960s discovery that all living beings use fundamentally the same genetic code.

As a result of these developments, Life Science departments or other disciplinary units began to replace the traditional departments by fusion and reorganization. Introductory biology courses began to replace introductory botany and zoology courses in the 1960s and the influential textbook "The Science of Biology" by Paul Weisz became widely used in introductory courses in North America.

Microbiology had separated earlier at many universities as a result of the recognition that the presence or absence of nuclei in cells was associated with other fundamentally different cell features and because of its medical bias. The French protistologist Edouard Chatton introduced the names 'prokaryotic' and 'eukaryotic' (with a 'c' instead of a 'k'; Chatton 1925), based simply on the absence or presence of nuclei, respectively (his 1938 publication is often given as the source, but this was a summary of earlier work; Chatton 1938). This fundamental distinction of cell types led to an alternative dualistic view of two kingdoms or Superkingdoms, Prokaryota and Eukaryota (e.g. Whittaker & Margulis 1978; Mohn 1984)

The Protistan Renaissance

The difficulty of assigning all things to the Lapides, Plantae or Animalia became increasingly evident in the mid- to late 19th century, especially between the latter two. Organisms, usually microscopic, combining features of both of the latter were discovered in the 19th century. As a result, it is now well known that John Hogg (1860) created a fourth kingdom, the "Regnum Primigenum" or Protoctista, meaning 'first beings' because they were belived to have arisen before plants and animals. Twenty-two years earlier, the great German microscopist Christian Gottfried von Ehrenberg had dogmatically asserted that they were tiny, 'complete' little animals ("Infusionsthierchen als Volkomene Organismen"), containing multiple stomaches (actually vacuoles) and other organs such as gonads (nuclei) and digestive glands (plastids). The 'cell theory' had not yet been formulated, and so there seemed to be no reason why such organs could not get smaller and smaller. In the 1840s, as the fundamental unitary nature of cells was being independently proposed by Mathias Schleiden and Theodore Schwann, Felix Dujardin showed that the cytoplasm (sarcode) of foraminiferans was not multicellular and Carl Theodor von Seibold established that they and other 'Protozoa' were unicellular.

As Whittaker & Margulis (1978) noted, many early classifications were essentially 'top-down' views of the living world, tracing plants and animals downword into plant-like and animal-like 'lower organisms'. The German evolutionist, embryologist, microscopist, philosopher, artist and long-jump champion of Jena University, Ernst Haeckel, who was the strongest 19th century advocate of the distinctness of unicellular organisms, had a 'bottom-up' view, looking at the diversity of the living world from the earliest cells. He proposed that many groups evolved separately from the plant and animal lineages and, in 1866, only 7 years after the publication of Darwin's "On the Origin of Species" in 1859, named them members of the "Protistenreich" or Protist Kingdom, the Protista. Collectively, they were referred to as 'protists' [see the review by Rothschild (1989) for the origins and uses of such names and Ragan (1997) for a more detailed history of the concept]. Although his tree showed them as a sister group to animals and plants, the choice of name and the text indicated that he thought they arose before animals and plants. At first, he included sponges and fungi but, in his later publications (Haeckel, 1894, 1904), he explicitly restricted Protista to predominantly unicellular organisms or colonies not forming tissues. Bacteria were (understandably) included, first as Mychota and later as Monerans. Corliss (1998) has recently reviewed the development of the concept of kingdom Protista extensively. Ernst Haeckel is clearly the 'Father of Protistology' as we know it.

Clifford Dobell (1911) seemed to champion this approach in his polemic, "The Principles of Protistology", but he was mainly concerned with countering the reductionist view of protists as mere unicells, emphasizing their functional completeness as organisms (like Ehrenberg), and his scope in this and later publications was clearly traditionally protozoological. Further, he championed an 'acellular' view of protists, rather than unicellular. A debate about the unicellularity of protists carried on for nearly half a century, summarized by Corliss (1989), but electron microscopy unequivocally showed that, with the possible exception of multinucleate cells, they are homologous with the single cells of multicellular eukaryotes, but do everything with only one such unit. In fact, the SET made clear that eukaryotic 'cells' with mitochondria are dyadic (digenomic) entities compared with prokaryotes and that those with plastids are triads (trigenomic; Taylor 1974). This genomic complexity, arising from intracellular symbioses, was believed to be the source of major evolutionary novelty by Ivan Wallin (1927) in the same work in which he proposed a symbiotic origin for the mitochondrion. He viewed this as a new form of speciation termed 'symbionticisim', considering it to be more important in evolution than mutation. These concepts have been evaluated by Taylor (1980, 1983, 1987), who concluded that the failed to convince others because of his excessive 'overselling' of symbionticisim, and Sapp (1995). Using Mereschkowsky's term 'symbiogenesis', Margulis & Cohen (1994) discussed its possible potential for innovation in a paleo-evolutionary context, and Margulis & Sagan (2002) have promoted its importance as a speciation mechanism to a wider audience.

Herbert F. Copeland tried to bring the Protoctista back formally in 1938 and, in an extensive, thorough book (Copeland, 1956), offered a complete, unified reclassification of 'lower organisms', but his efforts were to no avail. Werner Rothmaler's system, with Protobionta as a comparable category, was also greeted largely with indifference (Rothmaler 1948). Algae, fungi and protozoa were far too entrenched in their traditional departments to change radically and were formally supported by the International Codes of Botanical and Zoological Nomenclature. Twenty years later, the ecologist Robert H. Whittaker took the protistological baton and ran with it, reviving Haeckel's Kingdom Protista, together with a separate kingdom for Fungi (Whittaker 1959), following it with a major article introducing his Five Kingdom system in the usually conservative pages of "Science" (Whittaker 1969). However, both these and later versions, such as that with Margulis (Whittaker & Margulis 1978), still retained polyphyletic groups such as zoo- and phytoflagellates as precursor branches of animal or plant protist lineages. Emphasis was on macroclassification rather than on actual protist affinities.

These bold, perceptive individuals kept the protistan concept going but couldn't accomplish a general fundamental change in biologists' thinking. After all, all biologists received the same training in lower organisms', usually strong in only the material taught by one or other department. However, when Paul Weisz responded to the demand for an text to be used at the introductory university level, he responded with "The Science of Biology", in which he followed Copeland and Whittaker and used Protists as a major group (Kingdom) in place of Protozoa, Algae and Fungi and uniting the two former. However, no sooner had students passed beyond first year, their conceptual framework regressed 50 years, back to the traditional categories of Algae, Protozoa and Fungi.

Protozoa were traditionally classified as the simplest phylum of the Invertebrate, even by the most authoritative invertebratologist of the first half of the 20th century, the American Libbie Hyman. As recently as 1991, at the insistence of the editor, protozoa still were (Corliss 1991, with a caveat that they were included only for 'completeness'). Protist groups are still being added to the "Treatise on Invertebrate Palentology. In a contribution on Protozoa for a symposium on 'Invertebrate classification and phylogeny', organized by Hyman in 1959, John Corliss concluded that: 'the outlook for a good, defensible understanding of any phylogenetic relationships involving Protozoa is as discouraging as it ever was' (Corliss 1959, p.169)

Electron microscopy reveals cross-kingdom affinities in eukaryotes and roots the metazoa and Metaphyta (and Fungi)

Beginning in the late 1950s, Irene Manton pioneered that application of the transmission electron microscope (TEM) to study the ultrastructure of photosynthetic protistis, and she was soon joined by Dorothy Pitelka (heterotrophic protists) and others more concerned with the techniques themselves. A whole new, rich dataset became available for comparisons across all the eukaryotic group boundaries and, thanks to the observation of slices through many individuals simultaneously, it was possible to get a strong sense of the degree of variability to be expected in each. It also established the homology of many structures disguised under different names. For example, cilia and flagella were found to be identical in basic structure, with an extraordinary conservation of the '9+2' microtubular arrangement of basal bodies, and centrioles were clearly homologous with them. Bacterial flagella were shown to be not only much smaller but fundamentally different in structure, composition and function. The eukaryotic structures have historical precedence for the name: "Flagellaten" was a major protozoan cell type ever since Butschli (1880-1889), the Flagellata being one of four major Superclasses of the Protozoa in Grasse (1952), subdivided into phytoflagellates and zooflagellates. 'Flagellates' and 'flagella' have prevailed, despite attempts to replace the name of the eukaryotic structures with 'undulipodia' (all papers by Margulis since the 1970s) or the use of cilia for all of them (Hulsmann, 1992; all papers by Cavalier-Smith over the same period). If 'flagellum' is ambiguous, it is no more so than 'cell', and the context should leave no doubt as to the structure referred to.

The basic structures of nuclei, mitosis, mitochondria and chloroplast were soon shown to be essentially similar in all eukaryotes, both protists and multicellular organisms, but differed in details, some of which were group specific, e.g. internal or external spindles (the former apparentlly being earlier in origin). Golgi bodies and dictyosomes were shown to be fundamentally the same in animal and plant cells, respectively. At the same time, a whole new fine-structural dataset became available for comparative purposes that covered the whole, or most, of the range eukaryotes.

The outcome of the application of these data, reviewed by Taylor (1994, 1999) and Patterson (1999, 2000) among others, was no less than a revolution in our view of the relationships of the 'lower eukaryotes'. Many long-standing categories, such as Algae, Fungi, Protozoa, amoebae, heliozoans, Phytoflagellates, Zooflagellates, etc., were shown to be polyphyletic. As a result of the protistological approach, ignoring the old bundaries, new probable relationships were recognized, such as euglenoids with trypanosomes, based initially on their paddle-shaped cristae (Taylor 1976), but soon reinforced by several other features (Kivic & Walne 1984). Ciliates were linked with dinoflagellates on the basis of their cortical structural similarities (Taylor 1976; suggested also by Corliss 1975). Oomycetes resembled xanthophytes and other protists with compound flagella hairs (Taylor 1978). Corliss (1986) dated the 're-emergence of the field [protistology] as a respectable interdisciplinary area' from th mid-1970s, the same period in which the International Society for Evolutionary Protistology (ISEP) was founded.

The Five Kingdom/Two Superkingdom approach is intuitively appealing in its simplicity of concept, but is weak in its theoretical underpinnings and needs to be reconciled with the Three Domain (Bacteria, Archaea, Eukaryota) view arising from SSU rDNA trees.

Given the state of Knowledge prevailing in the 1970s and 1980s, a detailed new classification beyond that of Copeland (1956) would have had to undergo repeated conceptual and nomenclatural changes. Others have accepted the challenge, notably Cavalier-Smith (1981, 1993, 1998; and many other contributions up to this volume). This iterative approach should eventually lead to a more robust classification but, unfortunately, it generates new names and differing uses of old names as it goes. Corliss (1972) appealed for common sense and courtesy in such matters to avoid the proliferation of new higher taxa. The whole systematic question has been reviewed in detail by several authors, including Mohn (1984), Cavalier-Smith (1998), Corliss (1998, 2002) and Patterson (1999, 2000).

Another approach, currently in vogue, is to depict the relationships of many of the definable 75 or so protist lineages as a 'comb', in which most have no sister groups (e.g. Patterson 1999, 2000). However, the aggregation of groups according to mitochondrial crista types, as Patterson (2000) has noted, does seem to be remarkably concordant with several molecular datasets, including rDNA and mitochondrial DNA.

The literal meaning of the formal names of protist groups currently in use has been commented on elsewhere (Taylor 1999). I regret the continuation of anachronistic and inappropriate group-endings such as -zoa, -phyta and -mychota, except where they are literally apt. Also, the use of 'Protozoa' to include many more goups than usual, including some that are poly- or paraphyletic, seems unfortunate and likely to mislead the unknowing or unwary [see Patterson (2000) for a more detailed criticism and Corliss (2002), which includes a brief rebuttal].

Unquesitonably, it has been the rapid growth of molecular phylogenetics (Taylor 1994, 1999; Cavalier-Smith 1995; Patterson 2000) that has kept the interest in eukaryotic macro-evolution strong and the evolutionary protistan pot simmering; molecular sequencing continues to provide new insights, cement protistan relationships and raise new debates, particularly as different molecules and different methods yield differing results. 5S rDNA trees obviously had anomalous features, attributed to the small size of the molecule and the correspondingly small amount of *usale nucleotide sequence variation. LSU rRNA genes are so large and hypervariable in multiple regions that the latter need to be selectively removed in order to study group-level relationships (e.g. Ben Ali et al. 2001). In the 1980s and 1990s, SSU rDNA seemed to be 'just right' in size and information content for the latter purpose. In broad features, the trees it generated corresponded well with the main features of the TEM data (Sogin 1994; Sogin et al. 1996; Taylor 1994). Now, finally, it seemed that there was a molecule that could be used to resolve which of the 'absence/loss' choices was actually a primary absence. Some of the amitochondriate groups, such as the diplomonads and parabasalians and microsporidia, were basal in SSU rDNA trees. However, they were long branches and therefore potentially subject to a methodological artefact that made their placement suspect. In any case, new molecular evidence was emerging that revealed the presence of mitochondrial genes in the nuclei of these amitochondriate groups (Keeling 1998; Roger 1999).