© 2000, Annual Reports of the Zoological Institute RAS.
Andrew B. Shatrov
Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, St. Petersburg, 199034, Russia
In the study of morphology and ontogenesis of trombidiform mites, the author often came up against the concept of metamorphosis, since such a phenomenon is considered to be the integral attribute of the development of this group, not to mention other arachnids and arthropods. Therefore, the question of metamorphosis inevitably follows from the logic of research, carried out by the author. This report, however, is open to question and does not pretend to reveal all the aspects of the subject. Now the question may be formulated as follows. What is metamorphosis?
The problem of metamorphosis is quite complex and comprises different aspects from ecological and population up to molecular and genetic. In the West, at least two large volumes of collected papers on metamorphosis have been published - in 1968 and 1981, dealing with all these aspects, basically, however, with reference to amphibians and holometabolic insects.
The criteria and treatment of metamorphosis are quite different. If one proceeds from the most general ideas, it is necessary to recognize, that any development, in general, is of metamorphic character, since any organism during its development inevitably changes the form and size, particularly if a specialized larva, different from an adult, is observed in ontogenesis. Therefore, it is frequently admitted, that when the germ cells change this is evolution, and when the body changes this is metamorphosis (Wald, 1981). There are however, other, more special definitions of this phenomenon. Thus, metamorphosis is variously considered either as the process of transformation of an earlier stage to a later (Highnam, 1981), i.e. the polymorphism determined by the genome, underlying the irreversible switches of the organism adaptations from one of its functions to another (Wilbur, 1980), or as the complex process of intensive morphogenesis during one or two moults and realization of development potential of the adult form, when an animal during its life is adapted to more than one ecological niche (Locke, 1981, 1985; Sehnal, 1985). According to the definition of the author (Shatrov, 1991), metamorphosis is a cardinal change of the animal organization, basically determined by redistribution of morphological and functional value of different organs, which is thought to be the result of the influence of different environmental conditions on different phases of the animal ontogenesis. From the most general view, according to assumption of Bei-Bienko (1980), the nature of metamorphosis is that the developing individual undergoes essential transformation of morphological organization and biological features during its life. There are, certainly, many other points of view and definitions of metamorphosis, such as the ideas of divergent evolution of polymorphic organisms (Wigglesworth, 1954), convergent and divergent metamorphosis (Snodgrass, 1954, 1960), the origin of the pupal stage (Hinton, 1963), phyletic and adaptive larvae (Cohen & Massey, 1983), etc.
It can be seen, however, that the available definitions of metamorphosis, both specific, and also general, only describe from different positions the observable phenomenon of the unique change of morphology of an animal during its life but, as a rule, its reasons and nature remain unclear. Therefore, attempts of establishing ontogenetical meaning and importance of this phenomenon seems to be actual up to now. Here we are dealing not with the term, but with the sense of this specific phenomenon, which we denote as metamorphosis. Recognizing specificity of metamorphosis, on which Snodgrass especially insisted (Snodgrass, 1954), we, therefore, attribute to it unique features and should exclude from consideration other types of development.
In general, metamorphosis, as the change of the form of individual, can be developed only on the basis of more or less prolonged ontogenesis, including a number of stages, when the animal adapts to different environmental conditions during its development, and "the change of environment was a source of differences of adult insects from developing one", as Yezhikov (1929) has written. Actually, this statement concerns not only insects, but also other metamorphic animals, for example amphibians, implying in this case other ontogenetic and morphological material. The young stages of such a long ontogenesis very frequently, apparently, arose owing to disembryonization, i.e. hatching of an animal from the egg, by virtue of a number of reasons, at more earlier stages of development, in comparison with the initial ontogenesis. This results in formation of the larva, more or less distinguishable from the mature form. Therefore, it may be supposed, that the true larva in animal life history is a form of an animal in its individual development, which has arisen owing to disembryonization, unable to reproduction and develops various secondary, i.e. cenogenetic attributes which were not pronounced in adult ancestors. In other words, larva is expected to be a quite differentiated and specialized stage, but not underdeveloped at all, as one can sometimes think. In a larva, only organs of an adult animal still remain underdeveloped, but we do not know anything about these organs looking at larva. It is interesting to note, that Wigglesworth (1954) was one who, after Garstang (1928), has supposed an opportunity of independent evolution of insect's larvae due to natural selection. The same opinion has been evolved also by Grandjean (1957, etc.) and Andre (1988) concerning mites and their quiescent stases (calyptostases).
It is the transformation of such a differentiated larva into the adult form that is carried out by means of metamorphosis. Nevertheless, Snodgrass (1961) considered metamorphosis, in the narrow sense of this word, as only a temporary deviation of a winged insect back to a level of caterpillar or maggot (divergent metamorphosis), whereas its transformation into an adult insect he, on the contrary, referred to as retromorphosis (convergent metamorphosis), i.e. return of insect to its initial reproductive condition. In terms of evolution, this temporary retardation, as well as its source - disembryonization may be apparently explained by the necessity of development of an optimal trophic mode for a given ontogenesis with the purpose of more effective realization of imaginal functions, in particular functions of reproduction. Larva, in particular in insects, as is known, feeds and grows, in what its main ontogenetic destination is expected to be realized. In marine invertebrates, conversely, the larva very often, but not in all cases, serves for dispersal of species, whereas sessile adults feed. In other words, one can suppose that when growth, feeding and reproduction are observed in the same stage, metamorphosis will not be apparently pronounced. Conversely, when functions of feeding, growth and reproduction are distributed among different stages of ontogenesis, metamorphosis is expected to be developed. In any case, larva and, consequently, metamorphosis, are possible and arise, when there is not enough yolk storage found in the egg for fast achievement of an adult condition, as Schmalghauzen (1982) has particularly stated regarding vertebrate animals. But this definition is only another explanation of the phenomenon of disembryonization. Early hatching, nevertheless, may occur even if the egg is rich in yolk, which is a typical case in insects, according to Ivanova-Kazas (1997). Thus, a feeding of an embryo in these eggs appears, thus, ineffective for providing a complete imaginal life, and, as far as is known, insects do not have a lecitotrophic larva (Highnam, 1981).
Therefore, metamorphosis is a consequence of divergent ways of development of a larva and an adult animal in any ontogenesis, and the transition between a larval and an adult programs, in a parallel development model, is just metamorphosis proper in the classical interpretation, as Cohen and Massey (1983) have written. This is true particularly if a larva has not only phyletic features, as, for example, trochophore of polychaetes, but complex adaptive features, as larvae of holometabolic insects, i.e. at a secondary metamorphosis, according to assumptions of Yezhikov (1953). Thus, metamorphosis, in the morphological sense of this word, is a compression of development under environmental pressure to a minimum number of stages, ideally up to one (pupa). This is apparently resulted under conditions of morphological and ecological distinction between a larva and an adult animal (Sehnal, 1985), i.e. distinction in the programs of their development. In this case a larva, according to the theory of Berlese-Yezhikov, is considered to be an embryonic form which has undergone the process of disembryonization. And on the contrary, it is supposed, that embryonization, under conditions of initially prolonged ontogenesis, is favourable and even necessary for groups with a similar mode of life of a larva and an adult. If the environment is the same for different ontogenetic stages, the larva will become embryonized with inevitability and metamorphosis will be expected to reduce.
The immobility, partial or complete, of a pupa of holometabolic insects, having arisen on the basis of this distinction and resulted in restriction of its communications with external environment, provides further divergent adaptation of the larval and the adult forms incorporated, nevertheless, in the same life history (Williamson, 1992). Thus, the phase of pupa, limited always by only one stage, but initially having, probably, a number of stages (instars), is apparently thought to be a progressive stage, which divides more and more ecologically divergent stages of larva and imago.
From a general standpoint, it can be stated that the large number of stages (or instars), as, for example, in mites, denies the idea of metamorphosis and essential morphological difference between larval and adult stages, first of all on the basis of character of the internal organization. Moreover, larvae in mites, as may be apparently supposed, are not true larvae, but nymphs with significant retardation of adult organs and, on the other hand, obvious acceleration of the functioning tissues. Thus, the observable distinction between larva and imago, for example in holometabolic insects, would hardly be overcome, first of all from the ecological point of view, if all metamorphic processes would not be limited by only one stage, namely pupa, which is relatively independent of the external environment as well as of feeding.
The embryonic status of true larvae, as Yezhikov (1929) believed, determines an extraordinary development of their adaptive features owing to adaptation to the environment distinct from that of adult animals. The hypothetical transition of reproductive functions from imago to the larval stage (progenesis), in any animal group, would apparently result in an explosion of formation of new species and give rise to essentially new forms. It is possible to assert, therefore, that metamorphosis proper, is a rather specific phenomenon described by precise criteria, first of all of ontogenetic value. The author may suggest the following definition of metamorphosis. It is a relatively fast, irreversible and cardinal change of morphology and life pattern of an animal during its individual development that is a result of transition of reproductive functions from one differentiated and specialized form (larva) to another (adult animal or imago), provided that both these forms are well adapted to different environmental conditions and are capable of producing genetically divergent progenies. In all other cases, the development will not conform to the specific character and essence of metamorphosis.
In conclusion, the author can say that if he succeeds in awakening interest in this problem and showing its complexity even on the turn of millenium, the main purpose of this communication would be achieved.
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