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Basic morphogenetic processes in Hydrozoa and their evolutionary implications: an exercise in rational taxonomy
Abstract
Species-specific morphology in thecate hydroids is considered as a function of 2 fundamental morphogenetic characteristics: parameters of growth pulsations and the relation between the migratory activities of the endo- and ectodermal cells of the growing tips. Comparative, experimental and modelling data are presented suggesting that increases in the values of these parameters lead to gradual transformation of the narrow tubular rudiments of primitive thecates to the more transversely extended and later bilaterally symmetrical morphologies of advanced forms. There is a corresponding change in the mode of branching, from stolonal through alternate to opposite, with densely packed hydranths and hydrothecae. The relations between the traditional systematic approach to this group and the present ontogenetically based interpretation are discussed.
... At present, there is a limited number of attempts to analyse the group of modern multicellular organisms from the point of the priority of a limited number of developmental factors (parameters). In these works the authors analyzed morphogenetic parameters allowing constructing the system,covering and order ing the whole morphological diversity within a given taxon (Beloussov, 1975(Beloussov, , 1991Ubucata, 2001;Yagunova, 2005;Costello et al., 2008) or all animals on the whole (Beklemishev, 1974;Thomas et al., 2000). The logic of these works is based on the assumption that evolution of the group of organisms resets on the regular and consecutive transformation of a few basic ontogenetical variables. ...
... The logic of these works is based on the assumption that evolution of the group of organisms resets on the regular and consecutive transformation of a few basic ontogenetical variables. So it looks pos sible to reveal the basic morphogenetic processes which should remain essentially the same in all the representatives of a given group, being at the same time responsive to the genetically (as well as epigenet ically) controlled species generating transforma tions (Beloussov, 1991). ...
... Plumulariidae proposed by Von Schenck (Von Schenck, 1965), based on the shoot branching pattern, contains, in our opin ion, great numbers of convergences and parallelisms. Beloussov (1991) proposed the variant of the paramet ric system of thecate hydroids, based on the relation of two parameters of growth pulsations, the main mor phogenetic process in colonial hydroids. In 1993 Marfenin (1993) presented the sequence of increasing evolutionary complexity in the hydroid colony, based mainly on analysis of the morphological features. ...
The morphogenetic approach is applied to analyze the diversity of spatial organization of shoots in thecate hydroids (Cnidaria, Hydroidomedusa, Leptomedusae). The main tendencies and constraints of increased evolutionary complexity in thecate hydroids colonies are uncovered.
... The central rudiment continues to function as a shoot growing tip, while the lateral ones give rise to a pair of opposite hydrants. The detailed analysis of shoot internode development in D. pumila was used to model morphogenesis in colonial hydroids (Belousov, 1965(Belousov, , 1968(Belousov, , 1975Beloussov, 1991;Beloussov and Grabovsky, 2003) and to simulate the regulation of the structural pattern in hydroids (Berking et al., 2002;Berking, 2006). ...
... The pattern of the rudiment pulsations consecutively changes in the course of the morphogenetic cycle. After the initial stages, the rudiment demonstrates the typical growth pulsations pattern with a long extension phase, when the rudiment length remains constant (Wyttenbach et al., 1973;Belousov et al., 1984;Beloussov, 1991). The mean pulsation period is 11-13 min at 16-18°C. ...
... The internode formation in D. pumila and other thecate hydroids (Leptomedusae) with monopodial shoot growth was described many times using visual observation in transmitted light or histological data (Berrill, 1949;Belousov, 1965Belousov, , 1967Beloussov et al., 1972;Beloussov, 1973). The interpretation of morphogenesis during the tip growth and the corresponding morphogenetic models in hydroids proposed by Belousov et al. (Belousov, 1967;Beloussov, 1973;Beloussov and Dorfman, 1974;Beloussov, 1991;Beloussov and Grabovsky, 2003) relied on the assumption that the growing tip is a hollow structure with the walls composed of single layer possessing specific physical properties (thickness, elasticity, etc.). The proposed models were based on the assumption that the actual morphogenesis in hydroids is mediated by growth pulsations. ...
Two spatially separated processes underlie the growth and morphogenesis in hydroids (Cnidaria, Hydroidomedusa): (1) growth
pulsations of the terminal growing tips and (2) cell proliferation and migration in more proximal parts of the colony soft
tissues. Growing tips are morphogenetic elements of the colony that provide for the colony elongation and morphogenesis. In
thecate hydroids (subclass Leptomedusae) with highly integrated colonies and monopodial shoot growth, the initiation of the
lateral branches and hydranth rudiments looks like a periodic splitting of the growing tip into two or more rudiments. Published
descriptions and proposed models of this process assume that the splitting results from the formation of the furrows running
into the tip from its apical surface. In this study on a Sertulariidae species, we demonstrate that the visible process of
the tip splitting into several rudiments begins in its proximal part. At the same time, the inner ridges are initiated at
the skeleton lateral surfaces surrounding the growing tip. These ridges develop and grow along the proximodistal axis. Eventually,
the opposite ridges fuse, which splits the tip into several rudiments. We propose that the tip splitting into several rudiments
is impossible without the spatial regulation of the outer skeleton formation. This process explains many species-specific
properties of the shoot spatial organization in thecate hydroids such as the partial or complete fusion of the zooid skeleton
with the shoot stem skeleton, deflection of the distal parts of the zooid skeleton from the shoot stem axis, etc. The revealed
mechanisms considerably supplements and corrects the models describing morphogenesis in colonial hydroids.
... In this paper we took into account the series of papers by Berrill (1949aBerrill ( , b, c, 1950, and 'the theory of biological (embryonic) field' by Gurwitsch (1922) and his followers (Beloussov & Ostromova, 1969;Beloussov et al., 1972;Beloussov & Dorfman, 1974), including the only papers of their kind by Beloussov (1975Beloussov ( , 1991 on the 'parametric system of hydroids'. However, such works are still few in number, so the method of morphogenetic analysis in classification of forms remains poorly developed. ...
... As subdivision of the growing tip into separate hydranth and stem rudiments occurs earlier and earlier prior to differentiation of the hydranth (that is, toward the right side of Figs 5 and 6), the tip becomes asymmetric and unbalanced. The consequences of such a phenomenon are discussed in detail in the works by Beloussov (1975Beloussov ( , 1991. The asymmetry of the growing tip underlies the origin of diverse morphologies of different species. ...
A scheme of evolution of hydrozoan colony pattern is proposed based upon the consideration of macromorphogenesis. Four main
processes play decisive roles: (1) hard skeleton formation by soft tissues, (2) changes in duration of the growth phase relative
to the transition to differentiation in interdependent zones of growth, (3) ratio in growth rates between adjacent zones of
growth within the rudiment, the shoot, or the whole colony, and (4) spatial relationships among growth zones. The main tendency
in morphological evolution of the hydroids is an increasing integration of the colony as revealed by increasing complexity
of its structure. That is from a temporary colony towards the permanent one with highly organised shoots, as hydranths and
branches are localised in a strictly arranged manner. An analysis of diverse data allows one to state that the main morphogenetic
mechanism of increasing complexity in the hydroid colony is convergence, then fusion, of adjacent growth zones, a variant
of heterochrony.
Key words: hydroid colony, heterochrony, colony integration, Hydrozoa
... They can be distinguished most clearly within the growing tip and in the coenosarc just proximal to it ( Figure 7H). These are the parts of the stolon that permanently undergo active contraction and pulsation (Wyttenbach, 1968;Beloussov, 1973Beloussov, , 1991Kosevich, 2006). ...
Background
As the sister group to all Bilateria, representatives of the phylum Cnidaria (sea anemones, corals, jellyfishes, and hydroids) possess a recognizable and well-developed nervous system and have attracted considerable attention over the years from neurobiologists and evo-devo researchers. Despite a long history of nervous system investigation in Cnidaria, most studies have been performed on unitary organisms. However, the majority of cnidarians are colonial (modular) organisms with unique and specific features of development and function. Nevertheless, data on the nervous system in colonial cnidarians are scarce. Within hydrozoans (Hydrozoa and Cnidaria), a structurally "simple" nervous system has been described for Hydra and zooids of several colonial species. A more complex organization of the nervous system, closely related to the animals' motile mode of life, has been shown for the medusa stage and a few siphonophores. Direct evidence of a colonial nervous system interconnecting zooids of a hydrozoan colony has been obtained only for two species, while it has been stated that in other studied species, the coenosarc lacks nerves.
Methods
In the present study, the presence of a nervous system in the coenosarc of three species of colonial hydroids - the athecate Clava multicornis , and thecate Dynamena pumila and Obelia longissima - was studied based on immunocytochemical and ultrastructural investigations.
Results
Confocal scanning laser microscopy revealed a loose system composed of delicate, mostly bipolar, neurons visualized using a combination of anti-tyrosinated and anti-acetylated a-tubulin antibodies, as well as anti-RF-amide antibodies. Only ganglion nerve cells were observed. The neurites were found in the growing stolon tips close to the tip apex. Ultrastructural data confirmed the presence of neurons in the coenosarc epidermis of all the studied species. In the coenosarc, the neurons and their processes were found to settle on the mesoglea, and the muscle processes were found to overlay the nerve cells. Some of the neurites were found to run within the mesoglea.
Discussion
Based on the findings, the possible role of the colonial nervous system in sessile hydroids is discussed.
... Von Schenck (1965) analyzed the development and organization of shoots in the Plumulariida group based on the patterns of shoot growth and branching in this voluminous group of thecate hydroids. Beloussov (1975Beloussov ( , 1991 developed a classification of shoots in the colonies of thecate hydroids based on the morphogenetic mechanisms of their growth. ...
The high diversity of spatial organization of shoots in colonies of thecate hydroids (Cnidaria, Hydroidomedusa, Leptomedusae) is determined by their modular organization, which is characterized by the cyclic morphogenesis in the colony. It is attempted to show that evolutionary and ontogenetic changes in the spatial organization of hydroids of this group are based on the allometric growth of modules of colony shoots. An increase in size of a developing module provides prerequisites for earlier initiation of the growing tips of succeeding moduls (heterochrony). In some cases, heterochronies determined transition from cyclic to acyclic morphogenesis. The earlier emergence of new growing tips allowed integration of several primary modules into secondary modules, resulting among other things in changes in relative positions of primary modules (heterotopy). In complex colonies, these changes are traced in the ontogeny of a single colony.
About eight species are joined together into the genus named Obelia (Cnidaria, Medusozoa, Hydrozoa). However there are some species (about 10) attributed by some investigators to Obelia, and by others to three independent genera: Gonothyraea, Laomedea and Hartlaubella, which are nevertheless supposed to be closely related to each other and to Obelia. All the specialists agree that all these genera belong to a subfamily Obeliinae, family Campanulariidae. This review covers the topics: taxonomy, cell composition and cytogenetics, sexual reproduction and early developmental stages, growth and coloniality problems, feeding and digestion, other ecological problems, horizontal and vertical distribution, luminescence. It aims to demonstrate results gained by the specialists dealing with this group and to show the general trend of the continuing investigations. An appendix gives information concerning the Workshop, "Obelia as a dominant in epibiotic communities", which took place in September 1996 in St Petersburg.
We define the active memory of a developing system as the capacity to build its future from the reminiscences about its own immediately preceded finite past. We review several examples of active developmental memory, manifesting themselves in the morphomechanic reactions and in the properties of an ultraweak photon emission. By our suggestion, an active memory is an essential temporal component of the morphogenetic fields.
Cnidarians are primitive multi-cellular animals whose body is constructed of two epithelial layers and whose gastric cavity
has only one opening. Most cnidarians are colonial. Colonial hydroids with their branched body can be regarded as a model
for the whole phylum and are the most-studied cnidarian group with respect to developmental biology. Their colonies are constructed
by repetition of limited number of developmental modules. The new modules are formed in the course of activity of terminal
elements—growing tips of stolons and shoots. The growing tips of cnidarians, in contrast to those of plants, lack cell proliferation
and drive morphogenesis instead by laying down and shaping the outer skeleton and formation of new colony elements. Cell multiplication
takes place proximally to the growing tips. Branching in colonial hydroids happens due to the emergence of the new growing
tip within the existing structures or by subdivision of the growing tip into several rudiments. Marcomorphogenetic events
associated with different variants of branching are described, and the problems of pattern control are discussed in brief.
Less is known about genetic basis of branching control.
Changes in the form, structure and orientation of apical ectodermal cells during growth pulsations were studied in hydroid polyps by means of time-lapse microcinematography, light and electron microscopy. The growth pulsations were shown to be accompanied by changes in the volume of cells and the degree of their vacuolization. An “initial signal” is described which spreads in the beginning of every growth pulsation at rate not less than 3 mm/min, as a wave of cell reorientation which spreads in the proximo-distal direction at a rate 30-70 mk/min. A biomechanical model of participation of the contract and osmotic mechanisms in growth pulsations is proposed. The character and morphogenetic importance of the proximo-distal wave of cell reorientation is discussed.
1. Growth, morphogenesis and cell movements were studied in Obelia loveni, O. geniculata and Dynamena pumila with the use of time-lapse cinematography, visual observations of vitally stained objects and by histological techniques.
2. Growth pulsations with the period around 14min and the amplitude around 15 μm exist in Dynamena pumila and with the period 5–8 min and amplitude up to 5 μm in Obelia loveni. It was demonstrated that the rhythm of growth pulsations does not coincide with the rhythm of periodical contractions of the proximal part of coenosarc.
3. The distalwards movements of individual cells in the ectoderm of growing stems and hydranth rudiments are described. A considerable variability in the rates of movements of ectodermal cells has been demonstrated.
4. Different kinds of cell reorientations in developing rudiments are described. As a rule, they precede the alterations of growth directions or of rudiment shapes.
5. The mechanisms involved in deformations of epithelial layers are discussed.
6. The possibility of the existence of passive, elastico-plastic structures in the deforming epithelial sheets is suggested.
Comparative observations of stolon elongation in 19 genetic stocks of C. flexuosa reveal four respects in which such activity may differ, with each varying independently of the others. Two of these determine the stolonic growth rate: the duration of the growth cycle and the average growth per cycle. The stocks show a nearly continuous spectrum of these values, ranging, respectively, from 6.05 to 7.18 minutes and from maxima of 8.8 to 26.5 ?. The resulting maximal daily growth of the stocks varies from 1.9 to 6.2 mm. This rate is influenced much more by the stolon's growth per cycle than by its cycle time. The stocks vary also in the frequency of their repeating pattern of retractions from cycle to cycle; this "trough period" ranges from 2.5 to 7. Thus indirectly it may be concluded that the duration of each cycle of back and forth hydroplasmic flow in the stolon is also an inter-stock variable. Finally, the stolons of many stocks show a secondary forward surge of the tip following shortly after time crest of the cycle is reached, and the frequency of such "secondary peak" formation is also a stock characteristic. Its anatomical basis is cited. With respect to these four parameters of stolon growth activity alone, 18 of the 19 stocks are distinct from one another. It is suggested that several of these traits are so constant and easily measured that studies into their mode of inheritance should be feasible.
Cell orientation and intercellular changes accompanying growth pulsations (GP) have been studied in the marine hydroids Obelia longissima, O. loveni, and Dynamena pumila with the use of time-lapse filming, mechanography, optical microscopy, and electron microscopy. The extension phase of the GP was correlated with an increase in cell volume and the rotation of cells to a transverse orientation. Tip cells return to an oblique orientation during the retraction phase via a rapid (about 1 μm/second) distalward sliding of external cell poles. In most samples, a proximodistal wave of transversad cell rotations was observed within a period of 30–90 μm/minutes. In contrast, return to the oblique orientation is almost synchronous. The extension GP phase is correlated with extensive cell vacuolization and the retraction phase with fusion of these vacuoles into elongated channels opening into external space.
The extension phase was stabilized in hypotonic medium, isotonic medium with increased NaCl concentration, and by ionic transport inhibitors (which increase cytoplasmic concentration of Na+ and Cl−). GP are arrested in the retraction phase in hypertonic medium, isotonic medium with decreased Na+ and Cl− concentration, and by inhibitors whose decreasing cytoplasmic concentrations of Na+ and Cl− arrest GP in the retraction phase. These data point out the participation of osmotic mechanisms in the regulation of GP.
The growth and morphogenesis of Obelia loveni and Dynamena pumila asexual generation were studied. Their cell layers consist of tightly packed cells which are able to contract, to feorlent and slide upon one another while remaining at the same time anchored to elastic enveloping membranes. Both growth and morphogenesis are of pulsatory character due to coordinated periodic contractions and relaxations of cells. Cell contraction results in a normalization of cell orientations, an upward shift of the entodermal column, and an expansion of the rudiment's tip. Cell relaxation is accompanied by reverse deformations and an upwards shift of the ectodermal column. The spatial pattern of active and passive forces and supporting structures is ascertained.
The cyclic elongation of stolons and uprights in the hydroid Campanularia
- C R Wyttenbach
- S Crowell
- R L Suddith
Wyttenbach, C. R., S. Crowell & R. L. Suddith, 1965. The cyclic elongation of stolons and uprights in the hydroid Campanularia. Biol. Bull. 129: 429.
Morphogenetische Untersuchungen die nichtzellularen Gebilde bei Tieren
- K Saint-Hilaire
- K. Saint-Hilaire
Philosophical aspects of taxonomy
- A A Liubischev
- A. A. Liubischev
Vital observations of cell migrations in the hydroid Obelia loveni
- L V Beloussov
- L. V. Beloussov