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Biosystems, 10 (1978) 67--89 67 © Elsevier/North-Holland Scientific Publishers Ltd. PROBLEMS in the DEVELOPMENT of an EXPLICIT

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Biosystems, 10 (1978) 67--89 67 © Elsevier/North-Holland Scientific Publishers Ltd. PROBLEMS in the DEVELOPMENT of an EXPLICIT BioSystems, 10 (1978) 67--89 67 © Elsevier/North-Holland Scientific Publishers Ltd. PROBLEMS IN THE DEVELOPMENT OF AN EXPLICIT HYPOTHETICAL PHYLOGENY OF THE LOWER EUKARYOTES F.J.R. TAYLOR Department of Botany and Institute of Oceanography, The University of British Columbia, Vancouver, B.C., Canada V6T 1 W5 A semi-explicit arrangement of the lower eukaryotes is provided to serve as a basis for phyletic discussions. No single character is used to determine the position of all the groups. The tree provides no ready separation of protozoa, algae and fungi, groups assigned to these traditional assemblages being considered to be for the most part inextricably interwoven. Photosynthetic forms, whose relationships seem to be more readily discernable, are considered to have given rise repeatedly to nonphotosynthetic forms. The assumption that there are primitive "preflagellar" eukaryotes (red algae, non-flagellated fungi) is adopted. The potential value of mitochondrial features as indicators of broad affinities is emphasised, particularly in determining the probable affinities of non-photosynthetic forms, and this criterion is contra-indicative of a ciliate ancestry for the Metazoa. In the arrangement provided the distributions of chloroplast, mitochondrial and flagellar features match one another well, suggesting their probable co-evolution. 1. Introduction view of the relations of the algae, his "tree" contained numerous, not strictly representa- At the start of a paper of this type it is tional "twigs". Dodge {1974) was even less often appropriate to begin with an apt, but explicit, preferring to comment more on not very serious quotation to set the right taxonomic consequences. Leedale (1974) tone. In this instmace, the only quotation preferred to ignore the details of origin of which sprang readily to mind was "... For most of the numerous lines he recognised in fools rush in where angels fear to tread..." and his "Pteropod" and "Fan" arrangements. so the practice has been temporarily discon- Hanson (1976, 1977) tentatively suggested a tinued. few links in the ancestry of the animal-like There should be little need to explain the protists and lower Metazoans. Margulis value of phylogenetic trees in general, since (1969, 1974), on the other hand, has produced they form the basis of "natural" classifications some explicit arrangements in connection and serve as an aid to perspective for the with her proposals regarding the origin of the neophyte or specialist in another field or eukaryotes. highly detailed sub-branch. However, in order Detailed phyletic arrangements of these to provide relative stability to taxonomy such organisms will undoubtedly produce much trees should not be taken as highly authorita- dispute,but it can be argued that it is a valuable, tive when the state of knowledge is still in an progressive exercise and that it may be early, relatively incomplete stage. It can be pursued occasionally by some who enjoy this argued that to attempt an explicit arrangement "metascience" which, in the words of Stanier at this stage in the knowledge of the lower {1970) "can be considered a relatively harm- eukaryotes ("Protoctists") may be a waste of less habit, like eating peanuts, unless-it time and any resulting trees deceptively assumes the form of an obsession .... ". simplistic. For example, while Christensen This contribution is essentially an extension (1966) sketched some broad features of his of an earlier paper on the determination of 68 probable flagellate phylogeny presented at the knowledge of the degree of importance of the 28th Annual Meeting of the Society of various characters evaluated, and much of this Protozoologists at Corvallis, Oregon (Taylor, type of information is lacking. For example: 1976a). The aim of the previous paper was is the fact that an organism stores an alpha not only to discuss probable relationships but 1,4- rather than a beta 1,3- glucan profound also to reiterate the necessity for the use of or relatively trivial? Is the location of the information from several systems when storage within, or exterior to, a chloroplast of attempting to create such a phylogeny. Four major importance? Are differences in flagella main features were considered in that paper: hairs of major or minor importance? Clearly, mitotic systems, and flagellar, chloroplast and if one knew how many genes were involved mitochondrial structure. On the basis of in such similarities or differences, one might features of these four features it was possible have a more profound insight. But such to produce a "tree" which, although it had information will presumably be a long time various weaknesses, seemed to be a reasonable in coming. reflection of probable relationships or at least It is this lack of information which greatly detailed enough to be a target for criticism hinders attempts to follow two of Hanson's and modification. (1977) three "Rules" for phylogenetic When such an exercise is undertaken analysis, namely the consideration of the it is at first easy to view it as if it were an "total biology" of the organism in question, assembly-disassembly puzzle consisting of and the use of arguments based on probably numerous, oddly-shaped pieces which, when selective advantages to account for trans- the right sequence is found, will all fit together formations with time. For example, arguments neatly into a whole form. The problem at for the selective "advantage" or losses of first seems to be largely one of arrangement structure, and particularly the loss of photo- and sequences: when the right combination is synthesis, often seem excessively contrived. discovered, all the groups should form a The loss of mitochondria by protists living in structure with no incongruities. Only a brief low oxygen environments, such as the gut, experience should be required to reveal that seems reasonable as long as there is an ade- this is not where the main problem lies. quate alternative energy-producing system. Even though protists show many features Hanson notes the paradoxical side-by~ide which make them rather different from existence of highly reduced and highly elabor- metazoans and metaphytes (a fact which is ate flagellated forms in the insect hindgut. often overlooked in general biological discus- On the other hand a good reason for sions), nevertheless, they also show many increased phylogenetic study of the protists features, such as parallelism and convergent at this time is the wealth of ultrastructural evolution, which are likely to confuse the material which has become available since, would-be phylogenetic tree-maker (see for example, Pitelka's (1963) review of Hanson, 1976, 1977, for lengthy discussions protozoan ultrastructure. Ultmstructuml of this subject). Furthermore, much of the information is an invaluable aid to the deter- data can be confusing due to misinterpretation, mination of structural homologies in the wrong attribution to group, and variability protists, clearly indicating the original nature in features formerly thought to be conserva- of such curiosities as "parabasal bodies" and tive. "archoplasmic spheres" (golgi derivatives) and When all these features are considered, it is the "melanosome" of the dinoflagellate not surprising that almost any phyletic ocellus (a modified chloroplast). Processes arrangement is going to contain apparent such as mitosis have been much more accurate- inconsistencies. The evaluation of similarities ly described, and representatives of most and differences between groups requires some groups, including the rare and obscure, have 69 now been studied with electron microscopy. 2. Limitations of the fossil record It is time, therefore, to see if the application of this new information is useful for phyletic If any fossil record exists it should obvious- purposes. ly be consulted first in any such enterprise. It Qu arternar~ CENOZOIC Tertiary III " I C~otaoeous MESOZOIC Jurassic mm I Triassie iII .,m" ii ,,o Permian I if"~,-~mm I m Carboniferous Devon ian PALEOZOIC l *: °smm •Silurtan Or doyle :la n m ,-, mm '-1 Cambri au m: oOOo ml cmm ..~ .o B ITTE R SPRINGS ![' o- i': ° ,-- ~ Si nian •-- m - -- ~ ,~ o ,.,'---'=.,.. Isoo. --.--~'-~ - c ..... "--'=--= ~ E~ Proterozoio I ~ o,,o ? ? ? ? GUNFLINT 1 ~ ; t,.oo to e. o Gh. Aroheazt -zo 2 700 ra Catarahean Earth's crust 4500 Fig. 1. Minimal ranges for microfossil groups, compiled from various sources (e,g., Loeblich Jr., 1974; Sarjeant, 1974). The earliest widely acceptable eukaryotes occur in the Bitter Springs Formation 900 million years ago, MYA), but apparent budding in Huroniospora from the Gunflint Iron Formation (1900 MYA) has led to suggestions that it is a fungus (Darby, 1974) or red alga (Tappan, 1976). Eosphaera from the same formation has been attributed to the red algae (Tappan, 1976) or the volvocalean green algae (Kazmierczak, 1976). These differ- ing interpretations wel] illustrate the problems involved in assigning these early microfossils to extant groups. 70 may be surprising to some that there is a rich claim that euglenoids evolved only in the protist fossil record with probable eukaryotic Quaternary or Tertiary because their fossil unicells extending into the late Precambrian record is minimal, or that cryptomonads and (Fig. 1). The debate over the earliest eukar- many zooflagellates arose yesterday (no yotes (see for example the papers by Knoll record at all), or that non-loricate ciliates and Barghoorn, 1975; and Schopf and Zeller arose recently from loricate forms (tintinnids, Oehler, 1976), need not concern us here. their presumed fossils being known as "cal- However, assuming that these early fossils pionellids") because only the latter have a were eukaryotic, the problem of determining fossil record. to which group they might belong illustrates Even where skeletal structures exist there the limitations that are imposed upon the may be conditions under which they will not usefulness of the fossil record. Most of these be preserved in the sediments. For example, very early fossils are organic-walled spheres the calcareous plates (coccoliths) of the with little or no surface ornamentation.
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