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The Principle of Counter-Directional Morphological Evolution and Its Significance for Construction the Megasystem of Protists and Other Eukaryotes

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The Principle of Counter-Directional Morphological Evolution and Its Significance for Construction the Megasystem of Protists and Other Eukaryotes Protistology 2 (1), 6–14 (2001) Protistology April, 2001 The principle of counter-directional morphological evolution and its significance for construction the megasystem of protists and other eukaryotes Lev N. Seravin Biological Research Institute of St. Petersburg State University, St. Petersburg, Russia Summary Summing up, the following conclusions can be made. 1. Evolution of living systems follows the principle (law) of counter-directional morphological evolution, according to which both gradation and degradation of organisms can take place. 2. Combination of progressive and regressive changes in the structure of living creatures leads to the appearance of new taxa of any rank, including very high one (class, phylum, etc.). 3. In different groups of living organisms progressive and regressive morphological changes or their combination can result in the appearance of very similar but not identical taxa (e.g. sister taxa). The law of irreversibility of evolution should be substituted by a broader and more accurate law. It can be called the law of non-identity of similar structural transformations in different taxa of living organisms. Key words: morphological evolution, progressive and regressive evolution, Dollo’s law To construct a natural system of protists the role of Smith’s opinion, are always absent in the true Archezoa. not only progressive but also regressive morphological Thus only three phyla remained in this superkingdom: changes taking place in the process of those organisms’ Archamoeba, Metamonada and Microsporidia – unicellu- evolution should be taken into account. The validity of the lar eukaryotes which, in Cavalier-Smith’s opinion, are above statement can be conveniently demonstrated when initially devoid of mitochondria, chloroplasts, dictyosomes, considering changes upon the megasystem in the works of and any kind of microbodies. Yet soon, under the influ- Cavalier-Smith during the last 15 years. Proceeding from ence of convincing biochemical data, Cavalier-Smith a fairly widely spread point of view that the simpler the (1991, 1993) removes the Entamoebidae from the living organisms are the more originally primitive they Archezoa and includes them in the superkingdom Proto- should be, he united the macrotaxa including the flagel- zoa. lates and amoeboid organisms devoid of mitochondria into In the 90ies a series of studies on nucleotide sequences a single subkingdom Archezoa as a phylogenetically ini- and aminoacid sequences of heat shock proteins in a num- tial state for all the rest of the Protozoa kingdom ber of archezoan representatives appear, which showed (Cavalier-Smith, 1983). The investigator included four distinctly that the ancestors of those organisms had already phyla into this new taxon: Archamoeba (mastigamoebae, possessed mitochondria (Clark and Roger, 1995; Henze entamoebae, Pelomyxa palustris), Metamonada, et al., 1995; Bui et al., 1996). Cavalier-Smith (1996/1997) Microsporidia and Parabasalia (trichomonades, excludes the phylum Archamoeba from archezoans. He hypermastigines). Yet soon, Cavalier-Smith (1987, 1991, divides the Protozoa into two subkingdoms, Eozoa and 1993) drastically isolated Archezoa from all the other eu- Neozoa. He includes the Percolozoa, Euglenozoa and karyotes, elevating the rank of this taxon to that of kingdom Trichozoa phyla in the Eozoa, the Parabasalia being in- and even the superkingdom. At the same time he removed cluded as a subphylum into the Trichozoa. The subphylum the phylum Parabasalia from the Archezoa since its repre- Archamoeba (which also contains the class Entamoebae) sentatives possess hydrogenosomes – microbodies which appeared to be included in the phylum Lobosa, which was appear to be related to mitochondria. Besides, the distinguished from that of the Rhizopoda by this author. Parabasalia possess dictyosomes which, in Cavalier- Thus, after all this transformations, only two phyla, © 2001 by Russia, Protistology. Protistology · 7 Metamonada and Microsporidia remained in the gressive and regressive changes in the process of protists superkingdom and kingdom Archezoa. evolution would be considered. At the same time, this prob- Meanwhile some molecular biological studies have lem has long been under study on multicellular animals. been appearing in which it was shown that microsporidia Therefore let us turn to these studies. should be considered as related to higher fungi, simplified Acquaintance with the works of A.N.Severtsov (1912, owing to intracellular parasitism (Katiar et al., 1995; Keel- 1914, 1925, 1939), Schmalhausen (1969, 1983) and other ing and Doolittle, 1996). Therefore Cavalier-Smith (1998) authors who studied seriously the problem of the correla- removed the Microsporidia from the Archezoa. It would tion between progressive and regressive evolution did a seem that this taxon should be liquidated. Yet the investi- lot for my understanding of it but still does not give an- gator acted differently. He completely changed the whole swers to all the questions. One has to support the opinion Eukaryota megasystem, stopped dividing these organisms of those authors (e.g. Fetisenko, 1973 and Georgievsky, into superkingdoms and left only 5 kingdoms: Protozoa, 1985) who suggested that this problem is far from being Animalia, Fungi, Chromista and Plantae. All the former solved, mostly because the problem of regressive evolu- innovations were completely given up. The Protozoa king- tion is insufficiently worked out. Let us try to clarify the dom is now divided into two subkingdoms: Archezoa and reasons for such a situation and find some new approaches Neozoa. Cavalier-Smith abolished the Eozoa subkingdom to the analysis of the correlation between progressive and which he had established only half a year before (Cava- regressive changes in the process of the morphologic evo- lier-Smith, 1996/1997). To the archezoans, besides the lution of living systems. phylum Metamonada, the Trichozoa were also attributed. The complexity of the structural organization of dif- The Parabasalia, which some time before had been the ferent living creatures is so different that long before the first to be removed from the archezoans (Cavalier-Smith, appearance of the evolutionary idea there appeared a con- 1987, 1991), were placed as a subphylum into the ception of some “ladder of life” or “ladder of creatures” Trichozoa.. In the new system the Archamoeba were re- reflecting different levels of the organic world objects’ duced in rank to the non-taxonomical group “infraphylum” organization. For us this conception is usually associated in the new subphylum Conoza (within the phylum with the name the Swiss naturalist and philosopher Charles Amoebozoa). He transfers the Trichozoa phylum (together Bonnet (1720–1793). Lamarck (1809, 1935) showed in with the subphylum Parabasalia) from the Archezoa subk- his “Philosophy of Zoology” that only admission of the ingdom into the reestablished Eozoa kingdom existence of consistent plants and animal evolution allows (Cavalier-Smith, 1998). Therefore only the metamonades to the understand and explain rationally their gradation, remained within the archezoans. i.e. the existence of different levels of their organization Studies of the fine structure of Pelomyxa palustris (lat. gradatio – gradual elevation, gradus – step). (Goodkov and Seravin, 1991, 1995) have shown that this Charles Darwin, in chapter IV of his famous book “The protozoan possesses hydrogenosome-like microbodies and Origin of Species”, reports that when natural selection does dictyosomes. From the above it follows that P. palustris is not work organisms stay practically unchanged for a long not an archamoeba. The performed organellologic analy- time. Under the pressure of selection they evolve, compli- sis of those protozoa which Cavalier-Smith had then cating their organization. Yet the opposite process of the attributed to the Archezoa suggested that all the Archezoa simplification of the organism structure may take place. had sometime originated from ancestor forms which pos- He writes the following: “On the other hand, we can see, sessed mitochondria, i.e. the present protists devoid of these bearing in mind that all organic beings are striving to in- organelles had lost them secondary, having reverted to the crease at a high ratio and to size on every unoccupied or anaerobic or parasitical way of life. On the whole the analy- less well occupied place in the economy of nature, that it sis performed also showed that in the process of evolution is quite possible for nature selection gradually to fit a be- protozoans may lose mitochondria, chloroplasts, flagella, ing to a situation in which several organs would be dictyosomes, and all these organelles, taken together, in superfluous or useless: in such cases there would retro- this way approaching the proeukaryotes by their level of gression in the scale of organisation” (Darwin, 1872, p.98). organisation. Here it should be reminded that Margulis Following Ch.Darwin, I.I.Schmalhausen (1969) con- (1981), when P. palustris was hold to be devoid not only siders reverse evolution possible. I.I.Mechnikov in 1876 of mitochondria, but also of all the other main organelles (Mechnikov, 1950) calls regressive evolution reverse of the eukaryotic cell attributed this amoeboid organism movement in the development of organisms. It is true that to the forms evolutionary close to the proeukaryotes. Ch.Darwin (1898) repeatedly emphasized in his “Origin All the above testifies to the fact that regressive evo- of Species”
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