The Germ Similarity in Ontogeny of Ciliates (Ciliophora)
The paper deals with the regularities of ontogenesis of mobile and sessile ciliated protozoans. It is shown, that the germ similarity is characteristic both in mobile and sessile ciliates. The mechanisms of controlling of morphogenesis in ciliates are probably homologues with the controllers of earl...
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Інститут зоології ім. І.І. Шмальгаузена НАН України
2002
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irk-123456789-648512014-06-21T03:01:56Z The Germ Similarity in Ontogeny of Ciliates (Ciliophora) Dovgal, I.V. The paper deals with the regularities of ontogenesis of mobile and sessile ciliated protozoans. It is shown, that the germ similarity is characteristic both in mobile and sessile ciliates. The mechanisms of controlling of morphogenesis in ciliates are probably homologues with the controllers of early morphogenesis in multicellular organisms. The special statement for the case of law of germ similarity in unicellular eucaryots named "principle of tomits similarity" has been offered. В статье рассматриваются особенности онтогенеза подвижных и прикрепленных инфузорий. Показано, что зародышевое сходство проявляется как у подвижных, так и у сидячих форм. Механизмы регуляции онтогенеза у инфузорий и ранних этапов морфогенеза многоклеточных, вероятно, гомологичны. Предложена специальная формулировка закона зародышевого сходства для онтогенеза одноклеточных эукариот — принцип сходства томитов. 2002 Article The Germ Similarity in Ontogeny of Ciliates (Ciliophora) / I.V. Dovgal // Вестник зоологии. — 2002. — Т. 36, № 2. — С. 3–9. — Бібліогр.: 33 назв. — рос. 0084-5604 http://dspace.nbuv.gov.ua/handle/123456789/64851 593.17 : 591.3 : 575.86 en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
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The paper deals with the regularities of ontogenesis of mobile and sessile ciliated protozoans. It is shown, that the germ similarity is characteristic both in mobile and sessile ciliates. The mechanisms of controlling of morphogenesis in ciliates are probably homologues with the controllers of early morphogenesis in multicellular organisms. The special statement for the case of law of germ similarity in unicellular eucaryots named "principle of tomits similarity" has been offered. |
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Dovgal, I.V. |
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Dovgal, I.V. The Germ Similarity in Ontogeny of Ciliates (Ciliophora) Вестник зоологии |
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Dovgal, I.V. |
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Dovgal, I.V. |
| title |
The Germ Similarity in Ontogeny of Ciliates (Ciliophora) |
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The Germ Similarity in Ontogeny of Ciliates (Ciliophora) |
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The Germ Similarity in Ontogeny of Ciliates (Ciliophora) |
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The Germ Similarity in Ontogeny of Ciliates (Ciliophora) |
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The Germ Similarity in Ontogeny of Ciliates (Ciliophora) |
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germ similarity in ontogeny of ciliates (ciliophora) |
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Інститут зоології ім. І.І. Шмальгаузена НАН України |
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2002 |
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The Germ Similarity in Ontogeny of Ciliates (Ciliophora) / I.V. Dovgal // Вестник зоологии. — 2002. — Т. 36, № 2. — С. 3–9. — Бібліогр.: 33 назв. — рос. |
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Вестник зоологии |
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AT dovgaliv thegermsimilarityinontogenyofciliatesciliophora AT dovgaliv germsimilarityinontogenyofciliatesciliophora |
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2025-07-05T15:25:46Z |
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1836821141931425792 |
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Vestnik zoologii, 36(2): 3—9, 2002
© I. V. Dovgal, 2002
ÓÄÊ 593.17 : 591.3 : 575.86
THE GERM SIMILARITY
IN ONTOGENY OF CILIATES (CILIOPHORA)
I. V. Dovgal
Schmalhausen Institute of Zoology, vul. B. Khmelnits’kogo, 15, Kyiv, 01601 Ukraine
E-mail: dovgal@dovgal.kiev.ua
Accepted 4 May 2001
The Germ Similarity in Ontogeny of Ciliates (Ciliophora). Dovgal I. V. – The paper deals with the
regularities of ontogenesis of mobile and sessile ciliated protozoans. It is shown, that the germ similar-
ity is characteristic both in mobile and sessile ciliates. The mechanisms of controlling of morphogenesis
in ciliates are probably homologues with the controllers of early morphogenesis in multicellular organ-
isms. The special statement for the case of law of germ similarity in unicellular eucaryots named "prin-
ciple of tomits similarity" has been offered.
Key wo rd s : ciliates, ontogeny, germ similarity, recapitulation.
Çàðîäûøåâîå ñõîäñòâî â îíòîãåíåçå èíôóçîðèé (Ciliophora). Äîâãàëü È. Â. – Â ñòàòüå ðàññìàòðè-
âàþòñÿ îñîáåííîñòè îíòîãåíåçà ïîäâèæíûõ è ïðèêðåïëåííûõ èíôóçîðèé. Ïîêàçàíî, ÷òî çàðî-
äûøåâîå ñõîäñòâî ïðîÿâëÿåòñÿ êàê ó ïîäâèæíûõ, òàê è ó ñèäÿ÷èõ ôîðì. Ìåõàíèçìû ðåãóëÿöèè
îíòîãåíåçà ó èíôóçîðèé è ðàííèõ ýòàïîâ ìîðôîãåíåçà ìíîãîêëåòî÷íûõ, âåðîÿòíî, ãîìîëîãè÷-
íû. Ïðåäëîæåíà ñïåöèàëüíàÿ ôîðìóëèðîâêà çàêîíà çàðîäûøåâîãî ñõîäñòâà äëÿ îíòîãåíåçà îä-
íîêëåòî÷íûõ ýóêàðèîò – ïðèíöèï ñõîäñòâà òîìèòîâ.
Êëþ÷åâûå ñ ëîâà : èíôóçîðèè, îíòîãåíåç, çàðîäûøåâîå ñõîäñòâî, ðåêàïèòóëÿöèÿ.
Introduction
The concepts on the modifications during protist life cycle as ontogenesis have developed from the be-
ginning of twentieth century. It should be mentioned that B. P. Tokin (1934) was the pioneer has applied
the term "ontogeny" for the protist (ciliate) development. It is known, that the additional information for the
reconstruction of protist phylogeny can be obtained through the comparative study of their ontogenesis
(Eisler et al., 1995). In this connection it should be noted the peculiarities of the anlage of organelles in
protist ontogeny from the point of view of common regularities of individual development.
Although some specialists disclaimed the presence of ontogeny in not colonial protists (Sewertzoff, 1939),
the problem of the biogenetic law applicability to protist ontogenesis have been considered in detail in several pub-
lications (Hadzi, 1952, Dogiel, 1951, Dogiel et al., 1962, Corliss, 1968, Eisler et al., 1995, Foissner, 1996, etc).
In particular V. A. Dogiel (1951) marked that it is necessary to search the examples of recapitulations
in those protists that changed the mode of life during phylogenesis. The most typical case is the transition of
protists to the sessile mode of life. As most characteristic example of recapitulation in protist ontogeny the
formation of suctorian ciliated tomits have been mentioned. The similar occurrences also were marked in
peritrichs. In protists ontogeny there are some examples of the archallaxis, very few cases of the deviation
and greater examples of the anaboly.
In the review paper by M. Canella (1964) the study of ontogenesis have been considered as the useful
approach in construction of the natural system of infusoria. However this author have considered, that the
time history of infusoria ontogenesis may be essentially influenced with ecological and other poorly investi-
gated factors. This makes using of regularities of ciliate individual development for reconstruction of their
phylogeny difficult.
It is the A. V. Jankowski's (1972) opinion, that the ontogeny took place in any ciliates and begins from
the moment of anlage the fragment of tomit kinetom. The ontogeny finished to the anlage of the similar
fragment in a new generated trophont. A. V. Jankowski has recognized the following stages of ontogenesis in
ciliates (fig. 1, 2—I): tomit (the bud that separated from parental cell, or the cells are derived as a result of
binary fission); trophont (the feeding organism); tomont (the trophont, at which the anlage of tomit ciliature
is occurs); protomit (tomit that bounded with parental cell).
Using data on ontogeny, A. V. Jankowski (1972, 1973) have reconstructed the phylogeny of chonotrichs
and morphology of a hypothetical ancestor of these ciliates. For this author's opinion, the ontogeneses of cho-
notrichs, pilisuctorids, hymenostomats, thygmotrichs and rhynchodids are clear examples of anaboly.
I. V. Dovgal 4
Under the J. Corliss' (1968) opinion, the examples of recapitulations of ancestral characters might be
found in many taxa of protists. Especially it concerns the groups with complicatedly organized structures
such as pellicle or various skeletal structures. The such examples can be detected in mixosporidians (sculp-
ture of spore-valves), gregarine protozoa (diversified gametocyst membranes), coccidians, dinoflagellates
(structure of the thecal plates) and other flagellates (mastigont system).
However, the greatest number of similar examples is obtained at study of individual development of
ciliates that is connected with high complexity of pattern of their ciliature. As J. Beisson (1994, p. 15) has
marked "… ciliates face a true developmental problem: reconstruct the "imago" from part or remnants of its
pattern".
The peculiarities of ontogeny usually were applied for establishment of the systematic position of some
ciliates taxa (see Eisler et al., 1995). In fact, only applicability of the biogenetic law to protist phylogeny
reconstruction have been shown in majority of the above mentioned works.
As for recapitulations, they are analyzed at reconstruction of phylogeny of mobile infusoria, and in
such aspect the stomatogenesis (Corliss, 1968; 1979, Foissner, 1996) and reorganisation of cyrries at infu-
soria (Eigner, 1997) are considered only. The processes of swarmer metamorphosis have employed only at
reconstruction of chonotrich ciliates phylogeny (Jankowski, 1973). Finally, W. Foissner (1996) has applied
the Hennig's cladistic method to the ontogenetic data of ciliates.
In our opinion the matter what structures are recapitulated in the process of ontogenesis in sessile cili-
ates is still an open question. The purpose of the present paper is the attempt to estimate which regularities
of ontogeny both mobile and sessile ciliates can help to recognize their phylogenetic relationships.
Some regularities of ontogenesis in mobile and sessile ciliates
As indicated above, the recapitulations are usually discussed in the course of
stomatogenesis where mobile ciliates concerned.
The first stage of stomatogenesis is neoformations of kinetosomes that compose
the anlage of future oral ciliature. This anlage (or anarchic field) variously builds up in
different ciliate taxa. The different modes of stomatogenesis are correspondingly distin-
guished (Foissner, 1996). However, as marked J. Corliss (1968), these modes do not
relate directly to large taxa of ciliates. The stomatogenesis is by no reflects the stages of
phylogenesis. W. Foissner (1996) has discussed that no stomatogenetic mode can be
established for ciliates that lack an oral infraciliature (astomatous ciliates, suctorians,
rhynchodids, etc).
In the case of telokinetal stomatogenesis in which formation of the new oral appa-
ratus occurs by involvement of the anterior parts of somatic kineties (Corliss, 1979), it
is felt that the oral ciliature was formed by the anaboly. The stages of the such appara-
tus development in phylogenesis are recapitulated as the result. The same is probably
true (with some stipulations) for parakinetal stomatogenesis in which the anarchic field
is derived directly from some postoral somatic kineties of parental cell.
However in the case of buccokinetal stomatogenesis in which the new kineto-
somes have originate near the organelles of parental buccal apparatus (but not derived
from them) and, especially in the case of apokinetal stomatogenesis in which the new
oral kinetosomes have no pre-association with parental somatic or buccal kineties we
are probably dealing with results of archallaxis. The two last mentioned modes of oral
apparatus development accordingly give no way of phylogenetical reconstruction, but
testified only that there are possible affinities between taxa with the same mode of
stomatogenesis.
Except for stomatogenesis the process of shaping the complex pattern of somatic
ciliature in ontogeny also can tell us a lot about ciliate phylogeny. For example, in
P. Eigner's (1997) investigation of morphogenetic anlagen developments in the ventral
cirral rows in Oxytrichidae is shown, that their very similar pattern originated at least
from two different phylogenetic lineages.
During transition of protists to sessiling in connection with the motility loss the
problem of expansion appears inevitably. In such case the transition to irregular divi-
sion with formation of migratory stage saving organelles of locomotion was beneficial.
It gave additional benefits since the mother individual did not require transformation.
Thus it remained active and reserved the occupied localization that was important in
conditions of the topical competition (Dovgal, 2000).
The Germ Similarity in Ontogeny of Ciliates … 5
Therefore the evolution of sessile
protists life cycle took place at the
expense of the adding of new stages
(telotrochs, swarmers, etc) (i. e. ana-
boly after Sewertzoff). In its turn the
ontogenesis of sessile protists was
reduced to formation and develop-
ment of these migratory stages.
Hence the ontogeny of the sessile
ciliates included three stages: forma-
tion of the migratory stage, expan-
sion and choice of substrate and
metamorphosis of the migratory stage
after adhesion.
In majority sessile ciliates either
buccokinetal (in peritrichs) and
apokinetal stomatogenesis (in cho-
notrichs) is characteristic. As regards
the others morphogenetical proc-
esses, they pass is closely resembles
in the different groups (Dovgal,
2000). The common scheme of the
ontogenesis of sessile ciliates can be
considered by the example of cho-
notrichs (fig. 1).
The life cycle in the chonotrich
ciliates begins from the anlage the
fragment of tomit ciliature. Next the
generated tomit separating and settle
to the substrate after short-term
swimming. In the course of meta-
morphosis the swarmer of chonotrich
ciliate has gone through the some
stages that are similar to the assumed
ancestors (fig. 1, 4).
In the peritrichous ciliates the tomit (telotroch) is formed by pseudo-longitudinal
(Dogiel, 1951) (or more precisely enantiotropic (Foissner, 1996) binary fission of pa-
rental cell. The ontogenesis begins from the doubling of the peristome and the anlage
of the locomotor ciliature of telotroch. After the attachment to the substratum by
scopula the telotroch loses the locomotor ciliature and the stalk or lorica (if are pro-
vided) is secreted.
The budding starts in the suctorians with an invagination of a part of the cell cor-
tex. This parental fragment bearing some basal bodies that later give rise to the cilia of
the tomit (swarmer). Apart from kinetosomes the swarmer derived the nuclea and
anlages (axonemes) of tentacles (or completed tentacles) from parental cell. After the
settlement the adhesive organelle (i. e. stalk, etc) is formed (Bardele, 1970).
Discussion and conclusions
According to A. N. Sewertzoff (1939) biogenetic law is exhibited only when the
sequence of anlage of ancestral characters is recapitulated. As a rule such sequence is
exhibited if the evolution of ontogenesis of structures went on by way of anaboly of
consequent stages. As shows the literature data, this criterion was not directly applied
in the search for the possible recapitulations in ontogenesis of ciliates.
Fig. 1. The life cycle of Heliochona pontica: 1—2 – proto-
mit; 3 – tomit; 4 – the stage of phialochona (hypothetical
ancestor); 5—6 – metamorphosis of the swarmer; 7—8 –
conjugation; 9 – trophont.
Ðèñ. 1. Æèçíåííûé öèêë Heliochona pontica: 1—2 –
ïðîòîìèò; 3 – òîìèò; 4 – ñòàäèÿ ôèàëîõîíû (ãèïîòå-
òè÷åñêèé ïðåäîê); 5—6 – ìåòàìîðôîç áðîäÿæêè;
7 —8 – êîíúþãàöèÿ; 9 – òðîôîíò.
I. V. Dovgal 6
It is necessary to mark that as has been shown by A. N. Sewertzoff (1939) and
I. I. Schmalhausen (1969) the recapitulations are not characteristic for early stages of
ontogenesis. The archallaxis or deviations in development of structures are much more
spreaded.
If the morphogenesis of the mobile ciliates is conceived schematic (fig. 2—I), so it
can be seen that overall morphogenesis is actually finished in the stage of protomit.
The processes that can be considered as the recapitulations are seen at the same stage.
As with the other protists the ontogenesis of the sessile ciliates begins from the
moment of formation of derived cell rudiments, but unlike the mobile forms the de-
rived cell is usually a migratory stage (telotroch, swarmer, etc.). Accordingly, onto-
genesis of these protists is prolonged. At the first stage of ontogenesis (fig. 2—II) at
migratory stages organelles of locomotion, nuclear apparatus, organelles of a feed and
secretion of stalks developed. The derived cells receive the enumerated structures or
their rudiments from the parental cells. The second is stage of swimming and selection
of substratum. The last stage of ontogenesis is the metamorphosis of a migratory stage
after attachment. At this stage usually organelles of locomotion disappear (or they lose
the function of locomotion) where the adhesive organelles (in case of chonotrich cili-
ates also peristomal funnel) are formed.
In sessile ciliates the above mentioned sequence of ancestral characters is not ex-
hibited during forming of tomit. For example, oral structures of the tomits of cho-
notrichs are considerably simplified in comparison with the homologous structures of
their disteriid ancestor's. Tomits of sessile ciliates are more similar with derived indi-
viduals of free-swimming infusoria in some sense. The sequence of formation of adhe-
sive organelles, loricas, peristomal funnels, etc at stage of metamorphosis of a swarmer
Fig. 2. The ontogeny of mobile (I – after A. V. Jankowski, 1972 with changes) and sessile (II – by the exam-
ple of suctorians) ciliates (schematic): 1 – trophont; 2 – tomont; 3 – protomit; 4 – tomit; 5—6 – metamor-
phosis of the tomit; c – ciliature; i – infraciliature; at – anlage of the tentacle; t – tentacle; p – oral cilia-
ture; ap – anlage of the oral ciliature.
Ðèñ. 2. Ñõåìà îíòîãåíåçà ïîäâèæíûõ (I – ïî À. Â. ßíêîâñêîìó, 1972 ñ èçìåíåíèÿìè) è ñèäÿ÷èõ (II –
íà ïðèìåðå ñóêòîðèé) èíôóçîðèé: 1 – òðîôîíò; 2 – òîìîíò; 3 – ïðîòîìèò; 4 – òîìèò; 5—6 – ìåòà-
ìîðôîç áðîäÿæêè; c – öèëèàòóðà; i – èíôðàöèëèàòóðà; at – çà÷àòîê ùóïàëüöà; t – ùóïàëüöå; p –
ðîòîâàÿ öèëèàòóðà; ap – çà÷àòîê ðîòîâîé öèëèàòóðû.
The Germ Similarity in Ontogeny of Ciliates … 7
only can be considered as the recapitulations. But what represents then the text-book
examples with swarmers of suctorian and chonotrich ciliates?
In our opinion the emerging of some ancestral characteristics at the early stages of
morphogenesis (during formation of tomit) or the stages that are similar to the as-
sumed ancestors (during swarmer metamorphosis in sessile ciliates) are probably mani-
festations of the law of germ similarity.
If the concept of recapitulation has come into common use by protozoologists, so
the germ similarity essentially never discussed. The J. Corliss' (1968) paper is probably
unique protozoological work in which along with the recapitulations the law of embry-
onal similarity ("the fourth law") by K. Baer (1828) also has been mentioned. However
the author considers the Baer's law only as extended statement of the Haekkel's et
Muller's law.
In difference in the Russian literature (Sewertzoff, 1939; Schmalhausen, 1969;
Ivanova-Kazas, 1992; Dondua, 1993) was stated, that the law of embryonal similarity
and biogenetic law are provided by different mechanisms. N. Løvtrup (1986) have
reached to the same conclusions independently. This author proposed to discriminate
between "Baer's recapitulations" (i. e. embryonal similarity) and "terminal recapitula-
tions" (i. e. exhibited by anaboly after A. N. Sewertzoff).
It is necessary to stress that biogenetic law today was not taken seriously by em-
bryologists (Gilbert et al., 1997). While the regularities of morphogenesis which are fall
into the law of embryonal similarity recently was supported on the molecular level
(Dondua, 1993).
A. N. Sewertzoff (1939) was the pioneer has paid attention to phylogenetical
value of K. Baer's law. After A. N. Sewertzoff 's opinion, the sequence of characters of
adult animal emerging in early ontogenesis corresponds to the sequence of these char-
acters in phylogenesis. In contrast, the biogenetic law shows, in what sequence were
anlage the characteristics that existed in ancestors of the animal but than were substi-
tuted with other characters. Consequently, in the latter case the characters of adult
animal are not recapitulated.
The possible mechanisms of the embryonal similarity were discussed also with in-
voking of the data on plants development (Schmalhausen, 1969). Probably the Baer's
law applies to all cases of ontogenesis, including the individual development of pro-
tists (Dovgal, 1999, 2000).
The manifestations of this regularity are connected with the mechanisms of regula-
tion of morphogenesis. The developmental conservatism of early stages of ontogeny
promotes preservation (and manifestation) of ancestral characteristics (Schmalhausen,
1969).
At present the regulation of early morphogenesis linked with action of integrated
systems of gene interactions (Ivanova-Kazas, 1992, Dondua, 1993). These systems are
very conservative and are detected at quite diverged organisms. The homeodomains
represent these systems in the insects, vertebrates (Gilbert et al., 1997), plants and
yeasts (Kappen et al., 1993; Kappen, 2000; Zaraisky, 2001). It is the C. Kappen's
(1995) opinion that all eucaryotic organisms derive from ancestors that already pos-
sessed a homeodomains early during evolution. For our opinion, the detection of ho-
meodomains in yeasts (Kappen, 1995) testifies that homologues systems of early
morphogenesis regulation must exist both in unicellular (include protists) and multicel-
lular eucaryotic organisms. Consequently, the similar regularities must be reflected in
their ontogenesis.
External manifestations of the Baer's law in ciliates display certain specificity. In
all probability, the structures of cell cortex are of first importance in controlling of
morphogenesis.
For example, as the polarity of kineties in ciliate changes with micrurgy, the new
pattern is conserved during some following generations of up to conjugation. As
J. Beisson (1994) has discussed the cilia and their basal bodies which are anchored in
I. V. Dovgal 8
the cortex are of importance in ciliate morphogenesis (patterning). In our opinion the
instance of stomatogenesis is also suggests that the cortical structures has a dominant
role in morphogenesis.
Under A. Lwoff's (1990) hypothesis the modifications of the argyrome pattern in
suctorian ciliate Podophrya fixa (Muller) during budding, which was observed by the
author (Lwoff, 1950), is associated with rearranging of cortical proteins. It is the
A. Lwoff's (1990) opinion that this rearranging is the case by a Monod-Changeux-
Jacob principle. We believed, that the process reflects the function of the cortical
structures in controlling of morphogenesis without regard to its possible mechanism.
We can consider that there is good reason to propose the special statement of the
regularity of ontogeny in unicellular eucaryots that has been labeled as the principle of
tomits similarity. The I. I. Schmalhausen's (1969) definition of the Baer's law was used
as a basis for our statement:
1. The tomits display the certain similarity in the limits of phyla of protists at the
early stages of morphogenesis.
2. In the course of metamorphosis the tomits sequentially transforms from dis-
playing the common characters of the phylum to manifestation of increasable peculiar
characters. The characters which are indicative of the belonging of tomit to the certain
genus and species are developed at a later.
3. During metamorphosis the tomits of various representatives of one phylum are
more and more diverged.
The mechanisms of controlling of morphogenesis in ciliates (and most likely in all
protists) are probably homologues with the controllers of early morphogenesis in mul-
ticellular organisms. The specificity of individual development of unicellular eucaryots
is in the more essential governing of the cell cortical structures. The similar role in
multicellular organisms the cortex probably plays only at stage of the egg ooplasmic
segregation (see Kostyuchenko et al., 2000).
Therefore the tomit similarity may occur at the all stages of ciliate ontogeny and
gives an information for installation of the taxa relations. The investigation of this
regularity is probably the most perspective in solving of phylogenetical problems in
ciliates.
Acknowledgements
The author is grateful to the professor A. K. Dondua (St.-Petersburg, Russia) for valuable notes to the
manuscript of a paper and professor W. Foissner (Salzburg, Austria) for a fruitful controversy on the ontog-
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