Role of the skeleton in determination of the branching points in hydroid colonies

Colonial hydroids of the suborder Thecaphora have rigid outer skeleton that possesses species-specific shape of the colony elements. Organisation of the elements within a colony shows strict spatial patterning. The points of branching (emergence of the new growing tip) within shoots are strictly determined and show positive correlation with the place of the most pronounced curvature of the elements skeleton. As it was shown earlier, the shoot growing tip, after emergence, performs its program of functioning independently from the colony condition. Several modifications of experiments with grafting of the growing tip together with rotation around its longitudinal axis were fulfilled. As the result of such grafting the normal orientation of the formed skeleton was altered. In overwhelming cases of further tip growth and shoot development the new growing tip emerged in correspondence with new orientation of the formed skeleton. The orientation of the hydranth of the maternal shoot element had no effect upon the orientation of the new tip emergence after grafting. It is supposed that the place of the new tip emergence is regulated hierarchically. At first level, the interaction of the soft tissues with the skeleton has priority. Anisotropy of mechanical tensions within cell layers due to interaction with the skeleton at the point of its most curvature serves as a primary stimulus in the chain of events leading to the initiation of the new growing tip. If this does not work the intrinsic tissue property (polarity) determines the place of the tip emergence. Such two-level mechanism of determination of the place of the new tip emergence in sympodial shoots stabilises spatial organisation of the entire shoot and decreases the probability of epigenetic mistakes.     

Organizer regions in marine colonial hydrozoans

Organizers are specific tissue regions of developing organisms that provide accuracy and robustness to the body plan formation. Hydrozoan cnidarians (both solitary and colonial) require organizer regions for maintaining the regular body patterning during continuous tissue dynamics during asexual reproduction and growth. While the hypostomal organizer of the solitary Hydra has been studied relatively well, our knowledge of organizers in colonial hydrozoans remains fragmentary and incomplete. As colonial hydrozoans demonstrate an amazing diversity of morphological and life history traits, it is of special interest to investigate the organizers specific for particular ontogenetic stages and particular types of colonies. In the present study we aimed to assess the inductive capacities of several candidate organizer regions in hydroids with different colony organization. We carried out grafting experiments on colonial hydrozoans belonging to Leptothecata and Anthoathecata. We confirmed that the hypostome tip is an organizer in the colonial Anthoathecata as it is in the solitary polyp Hydra. We also found that the posterior tip of the larva is an organizer in hydroids regardless of the peculiarities of their metamorphosis mode and colony structure. We show for the first time that the shoot growing tip, which can be considered a key evolutionary novelty of Leptothecata, is an organizer region. Taken together, our data demonstrate that organizers function throughout the larval and polypoid stages in colonial hydroids.     

Mechanics of growth pulsations as the basis of growth and morphogenesis in colonial hydroids

Growth and shaping in colonial hydroids (Hydrozoa, Cnidaria) are realized due to the functioning of special colony elements, growing tips located at the terminuses of branched colony body. Unlike in plants, the growing tips of colonial hydroids are sites of active cell movements related to morphogenesis and lacking proliferation. The activity of hydroid growing tips is expressed as growth pulsations: cyclic repetitions of their apex extensions and retractions. The parameters of growth pulsations are species specific and related to the shape of a forming element. Here, the succession of cell movements and changes in mutual arrangement within the growing tip are described in detail at all pulsation phases. The role of the inner cell layer in the tip activity was demonstrated for the first time. Relationships between the growing tip parameters, length and diameter, and pulsations are discussed. A scheme is proposed for cyclic processes in both epithelial layers. An explanation is provided for the two-step mode of growth pulsations with relative independence of the main phases. It was proposed that successive activities of the tip ecto-and endoderm serve as driving forces provided there is a hard outer skeleton. This scheme makes it possible to explain some patterns of growth and morphogenesis in colonial hydroids, such as gradually increasing growth rate of a new tip and its maximum growth rate, differences in the parameters of growth pulsations between shoot and stolon tips, shoot base inclination towards the stolon tip, etc., and provides a basis for further improvement of the model of morphogenesis in hydroids.     

Mechanics of growth pulsations as the basis of growth and morphogenesis in colonial hydroids

Growth and shaping in colonial hydroids (Hydrozoa, Cnidaria) are realized due to the functioning of special colony elements, growing tips located at the terminuses of branched colony body. Unlike in plants, the growing tips of colonial hydroids are sites of active cell movements related to morphogenesis and lacking proliferation. The activity of hydroid growing tips is expressed as growth pulsations: cyclic repetitions of their apex extensions and retractions. The parameters of growth pulsations are species specific and related to the shape of a forming element. Here, the succession of cell movements and changes in mutual arrangement within the growing tip are described in detail at all pulsation phases. The role of the inner cell layer in the tip activity was demonstrated for the first time. Relationships between the growing tip parameters, length and diameter, and pulsations are discussed. A scheme is proposed for cyclic processes in both epithelial layers. An explanation is provided for the two-step mode of growth pulsations with relative independence of the main phases. It was proposed that successive activities of the tip ecto- and endoderm serve as driving forces provided there is a hard outer skeleton. This scheme makes it possible to explain some patterns of growth and morphogenesis in colonial hydroids, such as gradually increasing growth rate of a new tip and its maximum growth rate, differences in the parameters of growth pulsations between shoot and stolon tips, shoot base inclination towards the stolon tip, etc., and provides a basis for further improvement of the model of morphogenesis in hydroids.     

Basis of ontogenetic and evolutionary transformations of thecate hydroids

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.     

Morphogenetic evolution of hydroid colony pattern

A scheme of evolution of hydrozoan colony pattern is proposed based upon the consideration of macro-morphogenesis. 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.     

Regression and replacement of hydranths in thecate hydroids,and the structure of hydrothecae

In 1953 the author described a regression and replacement cycle of hydranths in Laomedea flexuosa and proposed that this is a common feature of thecate hydroids. Here examples are presented of replacement of hydranths in species from 5 families of thecates, but it has not been demonstrated that this is as common as had been thought. More continuous studies are needed. A brief consideration is given to the origin of hydrothecae and their development.     

Basic morphogenetic processes in Hydrozoa and their evolutionary implications: an exercise in rational taxonomy

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.     

Morphogenetic foundations for increased evolutionary complexity in the organization of thecate hydroids shoots (Cnidaria,Hydroidomedusa, Leptomedusae)

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.     

FMRF-amide immunoreactivity pattern in the planula and colony of the hydroid Gonothyraea loveni

Gonothyraea loveni (Allman, 1859) is a colonial thecate hydrozoan with a life cycle that lacks a free-swimming medusa stage. The development from zygote to planula occurs within meconidia attached to the female colony. The planula metamorphosis results in the formation of a primary hydranth. The colony then grows by development of new colony elements. In the present work, we studied the temporal pattern of the formation of FMRF-amide-positive cells during embryogenesis, in larvae and during early colony ontogeny. FMRF-amide-positive cells appear in the planula only after its maturation. However, they disappear after planula settlement. For the first time, we show that neural cells are present in the coenosarc of the hydroid colony. We also trace the process of neural net formation during the development of a new shoot internode of the G. loveni colony.     

The principles of functioning of the distribution system in colonial hydroids

Experimental study of the hydroplasmic flows in Gonothyraea loveni (Allm., 1859) uncovers a hydraulic principle determining the functioning of a pulsatory-type distribution system in colonial hydroids during metamorphosis of the planula, formation of the primary shoot, and colony growth. The absence of regulation of the hydroplasmic movement cycle is demonstrated.     

Relay-ray way of hydroplasm movement in hydroid colonies

In this study, we continued the investigation of the distribution system of colonial hydroids in the course of its development, starting with its emergence during the planula metamorphosis and ending with the formed colony. The hydroplasmic stream system of two species of colonial hydroids—Perigonimus abyssi G.O. Sars, 1874, and Stauridia producta Wright, 1858—was studied. We found that the main principle by which hydroplasma moves in these colonies, which form no shoots, is the relay-race from one hydranth to another through a stolon fragment connecting them or it moves past the neighbouring hydranth to the next one, etc. We show that the efficiency of the conducting (distribution) system does not depend on the level of complexity of the colonial structure. The results of this study confirm the absence of general colonial processes of integration and self-regulation in hydroid polyps.     

SIF, a novel morphogenetic inducer in hydrozoa.

By analogy to processes in angiogenesis (blood vessel formation), the development of the stolonal network in colonial hydrozoa involves stimulation of branching and mutual chemotropic attraction of the growing branches by means of soluble morphogenetic factors. We have identified a glycoconjugate of about 20 kDa, termed SIF (Stolon-Inducing Factor), which induces the formation of stolon branches when applied locally. Micropipettes ejecting SIF mimic the inducing action of stolon tips, the putative sources of SIF. When whole animals are exposed to SIF, stolons sprout not only from the base of the polyps but also from abnormal sites along the entire body, even from the head. In addition, the polyp (hydranth) secretes a chitinous periderm which, in the species under investigation, normally envelops stolons but not hydranths. At high SIF doses the whole hydranth is transformed into stolon tissue. The factor has been isolated from conditioned medium and from butanol extracts of Hydractinia echinata and Podocoryne carnea.     

Growth and reproduction of an estuarine population of the colonial hydroidCordylophora caspia (Pallas) in the northern Baltic Sea

Growth and reproduction of the colonial hydroidCordylophora caspia were monitored during the breeding season in natural conditions. In 1987, a life history study was carried out on the upright stems of the main stolon. Mean size of uprights varied cyclically. The first peak coincided with the peak number of sexual hydranths, after which the mean upright length decreased, possibly indicating somatic costs of sexual reproduction. Extrinsic factors like flooding may also have contributed to cyclical changes in upright size. In 1988 and 1989, colonies were reared on experimental plates in the estuary. In 1988, colonies grew until mid July, after which they regressed to a dormant condition and then started growing again in mid August. Predation and space competition are discussed as possible causes for this dormancy in the middle of the growing season. In 1989, colonies grew continually, with the exception of a decline in colony biomass and number of feeding hydranths at the end of July, just following the peak of sexual reproduction. Sexual reproduction started in the early stages of colonial development for all years. During early summer,C. caspia allocated resources simultaneously in colonial growth and sexual reproduction. However, sexual reproduction had a clear peak in mid summer, and thereafter sexual reproduction ceased while colonial growth continued.     

The growth and degeneration of the hydroid Sertularia perpusilla,an obligate epiphyte of leaves of the seagrass Posidonia oceanica

The hydrorhizae of Sertularia perpusilla colonies that originate from stolon attachments initially grow up and down Posidonia leaves. After a short time the distal hydroid tissue degenerates concurrently with the downward growth of the proximal hydrorhiza onto younger sections of the leaves. Consequently the hydroids move down the leaves which grow upward from a basal meristem. In situ inversion of leaves had no effect on either the orientation or the rates of growth and degeneration. This indicates that orientation may be in response to age related features of leaf tissue rather than to light, gravity or water movement, the directions of which were reversed by inverting the leaves. However, orientation of growth of new hydroids from attached stolons is immediate, probably before the hydroid colony is long enough to be able to detect an age gradient. This paradox could be explained if initial orientation were based on the direction of gravity or light but subsequent growth were directed along the age gradient. For hydroids in the size range studied there was a relation between growth rate and number of hydranths. Thus growth rate may be limited by food rather than by there being only one growing tip of the hydrorhizae.     

Autoaggressive,multi-headed and other mutant phenotypes in Hydractinia echinata (Cnidaria: Hydrozoa)

In an inbreeding program conducted with the colonial hydroid Hydractinia echinata, each F1 mating produced up to 50% F2 offspring displaying an aberrant, clone-constant phenotype, hence referred to as mutant strain. In autoaggressive strains, in one or several areas of the colony autoreactive stolons direct their aggressive devices (stolon tips filled with cytotoxic stinging cells), normally used to kill allogeneic competitors for living space, towards neighboring stolons or polyps (hydranths) of their own colony. In these areas tumor-like masses of self-aggressive stolons were formed, in severe cases causing the death of the colony. Based on previous genetic studies, the interpretation proposed here attributes autoaggressive behavior to a mosaic-type alternative expression of arl (allorecognition) alleles in heterozygous individuals. Developmental mutant strains termed He-mh form supernumerary heads during regeneration and normal development as well. Common to all He-mh phenotypes isthe production of additional headsalong the bodycolumn of fully-grown polyps. The heads give rise to complete hydranths connected by a tube that derives from the gastric region of the original polyp and eventually transforms into a stolon. In bastol strains, polyps convert the basal region of their body column into a periderm-covered stolon from which the residual apical hydranth detaches. Colonies expressing both the He-mh and the bastol (bst) phenotype frequently lose detaching multi-headed hydranths and the colony disintegrates. The large number of mutant F2 offspring reveals high genetic variability in Hydractinia.     

A shoot meristem-like organ in animals; monopodial and sympodial growth in Hydrozoa

Thecate Hydrozoa produce stems from which polyps branch off. Similar to plants these stems form in two ways, either in a sympodial or in a monopodial type of growth. In the latter group a terminal organ develops which has similarities to a shoot apical meristem of higher plants: it elongates without a further differentiation. Similar to leaf formation in plants, thecate Hydrozoa produce polyps in a repetitive manner. This process continues during the whole life of the animal and has not yet been found to be limited by internal mechanisms. We studied the monopodially growing thecate Hydrozoon Dynamena pumila and suggest that the stem tip, the apical shoot meristem-like organ, is a polyp primordium hindered to develop into a polyp by the laterally developing polyps.     

Cell Movements Associated with Terminal Growth in Colonial Hydroids

A series of studies into the nature or leimiual growth movementsin hydroids (chiefly the thecate Campanularia) is reviewed.Both stolon and pedicel tips of all hydroids observed grow byan endless repetition of "growth cycles." In thecate stolons,the geometry of the tip's excursions is relatively simple andsuccessive cycles are predictable in their duration and percycle growth. Conversely, athecate stolons are much more complexor variable in each of these respects. In Campanularia bothcycle time and per cycle growth differ among genetic stocks. Such environmental or environment-related factors as temperature,organic contaminants in the sea water, and the nutritive conditionof the colony each affect cycle time and/or per cycle growth.Also, ingestion of a large meal temporarily inhibits the retractionsthat characterize most growth cycles. Growth movements are a property of the stolon tip, since isolatedtips less than 0.5 mm long move in basically normal fashion.However, two aspects of the cycle are, modified by more distantregions: the cycle is accelerated by a pacemaker lying 0.5 to2.0 mm from the tip, and the extent of each cycle's retractionphase is determined by intrastolonic pressure generated by hydroplasmicflow. Certain neuroinhibitor drugs duplicate in intact stolonsthe cycle changes seen in surgical isolates. Synchronized with each growth cycle is a pattern of epidermalthickening and thinning at the stolon tip, this layer beingthinnest just after the crest and thickest about two-thirdsof the way through the cycle. Cells behind the tip also movein relation to the growth cycle, generally approaching the tipduring epidermal thickening and retreating during epidermalthinning. Several types of metabolic inhibitors markedly affect the stolonicgrowth movements, indicating the need of oxidative metabolismand of protein synthesis using a short-lived mRNA for the tip'sactivities. Campanularia pedicel growth cycles differ from stolon growthcycles in having a shorter and more variable duration, a lesserper cycle growth, and a shallower retraction phase, with changesin these features along the length of the pedicel correlatedwith changes in the type of growth occurring. These studies and those of other investigators are related,their contributions to our understanding of elongation are discussed,and persisting problems are highlighted.     

Low-molecular-weight factors from colonial hydroids affect pattern formation

Summary Two morphogenetic factors have been isolated from tissue of colonial hydroids. Both exert strong effects on pattern formation during metamorphosis, regeneration and colony development. Polyp-inhibiting factor (PIF) is a bivalent inhibitor which strongly affects head and bud formation but acts weakly on stolon branching. Proportion-altering factor (PAF) is a distalizing factor. It counteracts the formation of stolon and promotes the formation of head structures during metamorphosis and regeneration. PIF and PAF antagonistically influence the spatial arrangement of polyps within a colony. They are capable of dislocating structures and thus appear to interfere with or are even part of the pattern-controlling mechanism. Both factors are of low molecular size (about 500 daltons), hydrophilic and probably not peptides.