The development and evolution of hydrozoan polyp and colony form

Hydrozoans represent an extremely diverse group of mostly colonial forms. Despite this tremendous diversity, many of the morphological differences between hydrozoan species can be attributed to simple changes in the relative position of regions/structures along the axes of the polyp and the stolon or hydrocaulus from which polyps bud. Many genes have been implicated in the specification of positional information along the axis of the polyp. Knowledge from these studies in Hydra, and from comparative studies in Hydractinia polyp polymorphs, suggests that evolutionary changes in the regulation of axial patterning genes may be a prominent mechanism underlying hydrozoan evolution. Despite the paucity of interspecies comparative expression information, hypotheses can be formulated about the role of developmental regulatory genes in hydrozoan evolution from information available from Hydra.     

Control of metamorphosis and pattern formation in Hydratinia (hydrozoa,cnidaria)

Hydractinia echinata is a marine colonial hydroid, a relative of the more widely known Hydra. In contrast to Hydra, embryogenesis, metamorphosis and colony growth in Hydractinia are experimentally accessible and therefore, provide an ideal model system for investigating the biochemical basis of pattern formation. In particular, the processes involved in the transformation of the drop-shaped freely swimming larva into a sessile tube-shaped polyp are easily monitored, because this transfomation can be induced by application of various substances. Our results indicate that the internal level of S-adenosylmethionine (SAM), potentially the most important methyl donor in transmethylation processes, plays a key role in the onset of metamorphosis. It is also proposed that the internal level of SAM plays a pivotal role in the proportioning and spacing of polyps within the colony.     

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.     

THE COORDINATION OF POTENTIAL PACEMAKERS IN THE HYDROID TUBULARIA

Sectioning experiments and electrical recording indicate thatthere are many potential pacemakers in polyps of the hydroidTubularia. Functionally the pacemakers are organized primarilyinto pacemaker systems, groups within which there is tight coupling.The different pacemaker systems of a polyp are loosely coupledto one another. There are two principal systems in Tubularia,one in the polyp neck (the NP system) and one in the hydranth(the HP system). In addition, there are pacemakers controllingactivities of individual tentacles. Activity in the NP systemis usually not associated with observable polyp behavior. HPsystem activity is correlated with behavioral responses termedconcerts. Concerts are probably digestive activities; they resultin the mixing of food being digested and the distribution ofthe products of this digestion. The NP systems of polyps ona colony are loosely coupled to one another through one of thethree conducting systems found in Tubularia stalks. The loosecoupling between NP systems of polyps on a colony and the loosecoupling between NP and HP systems within single polyps resultsin there being some coordination of concert activity throughouta colony.     

Allorecognition in the Colonial Marine Hydroid Hydractinia (Cnidaria/Hydrozoa)

The colonial marine hydroid Hydractinia has a sophisticatedallorecognition and effector system. Unlike many unitary organisms(i.e., vertebrates) which lack a current context for allorecognition,there is the potential for strong selection pressure for allorecognitionand response in Hydractinia. Hydractinia colonies use allorecognitionin intraspecific competition for two dimensional space; spaceis an absolute requirement for Hydractinia to successfully completeits life-cycle and thus interactions for space are of centralimportance for Hydractinia. Studies of the mechanisms, molecules,and genes involved in allorecognition in Hydractinia may contributeto our understanding of the evolution of allorecognition inthe metazoa.     

ECOLOGICL ASPECTS OF THE MORPHODYNAMICS OF SOME HYDROZOA

The specific architecture of a Hydroid polyp or a colony is,morphologically speaking, not a stable entity, because it issubjected to an incessant turnover and renewal at both cellularand higher levels. A continuous morphogenetic activity is inmany cases (e.g., Hydra) necessary for the maintenance of theshape and size of the individual polyp, because it has to compensatean equally continuous loss of cells at the level of the tentaclesand at the base of the polyp. Colonial species, such as Tubularia,Campanularia, and others, show regression-replacement cycles,some of which are conditioned by endogenous factors, while othersare released by ecological factors, such as environmental stresses.In all these morphodynamic events, regeneration plays an importantpart. It is an expression of the morphogenetic plasticity ofthe hydroid polyp, just as is asexual reproduction, anothercategory of morphodynamic elforts these organisms are subjectedto.     

Phenotypic plasticity and morphological integration in a marine modular invertebrate

Background  

Colonial invertebrates such as corals exhibit nested levels of modularity, imposing a challenge to the depiction of their morphological evolution. Comparisons among diverse Caribbean gorgonian corals suggest decoupling of evolution at the polyp vs. branch/internode levels. Thus, evolutionary change in polyp form or size (the colonial module sensu stricto) does not imply a change in colony form (constructed of modular branches and other emergent features). This study examined the patterns of morphological integration at the intraspecific level. Pseudopterogorgia bipinnata (Verrill) (Octocorallia: Gorgoniidae) is a Caribbean shallow water gorgonian that can colonize most reef habitats (shallow/exposed vs. deep/protected; 1–45 m) and shows great morphological variation.     

A novel mode of colony formation in a hydrozoan through fusion of sexually generated individuals

Coloniality, as displayed by most hydrozoans, is thought to confer a size advantage in substrate-limited benthic marine environments and affects nearly every aspect of a species' ecology and evolution. Hydrozoan colonies normally develop through asexual budding of polyps that remain interconnected by continuous epithelia. The clade Aplanulata is unique in that it comprises mostly solitary species, including the model organism Hydra, with only a few colonial species. We reconstruct a multigene phylogeny to trace the evolution of coloniality in Aplanulata, revealing that the ancestor of Aplanulata was solitary and that coloniality was regained in the genus Ectopleura. Examination of Ectopleura larynx development reveals a unique type of colony formation never before described in Hydrozoa, in that colonies form through sexual reproduction followed by epithelial fusion of offspring polyps to adults. We characterize the expression of manacle, a gene involved in foot development in Hydra, to determine polyp-colony boundaries. Our results suggest that stalks beneath the neck do not have polyp identity and instead are specialized structures that interconnect polyps. Epithelial fusion, brooding behavior, and the presence of a skeleton were all key factors behind the evolution of this novel pathway to coloniality in Ectopleura.     

Intraspecific contact and egg production in the massive coral Goniastrea aspera in Okinawa, subtropical Japan

The effect of intraspecific contact (Contact) on egg production was examined in the massive coral Goniastrea aspera in Okinawa, subtropical Japan. The contact was non-aggressive without damaging soft tissues each other. Within Contact colonies, polyp volume, polyp fertility (%polyps with gonad), and NE/PV (number of eggs per polyp volume) were significantly smaller in marginal (Mg) polyps without direct intraspecific contact than other polyps, but no difference was found between non-marginal and Mg-Contact (marginal with direct intraspecific contact) polyps. Comparisons of non-marginal polyps (non-marginal and Mg-Contact polyps were combined in Contact colonies) between Non-Contact and Contact colonies showed that fertility and NE/PV were significantly larger in Contact colonies than in Non-Contact colonies, but polyp volume were not different significantly. Further analyses dividing colonies at Non-Contact maturation colony size (60 polyps) revealed that fertility and NE/PV were significantly larger in Contact colonies than in Non-Contact colonies only in the small colonies (<60 polyps), indicating that the intraspecific contact promoted sexual maturation at smaller colony size; one polyped Contact coral was also reproductive. The lack of correlation between polyp volume and NE/PV in the small Contact colonies, and the similarity of NE/PV in non-marginal and Mg-Contact polyps within a colony, suggest that the maturation at smaller size in Contact colonies is realized by reproductive integration of polyps at the colony level. The present results show that size-structured populations such as colonial corals may show phenotypic diversity in key demographic parameters, such as reproductive output, dependent on ecological conditions.     

Expression of a Gsx parahox gene, Cnox-2, in colony ontogeny in Hydractinia (Cnidaria: Hydrozoa)

The ontogeny of colonial animals is markedly distinct from that of solitary animals, yet no regulatory genes have thus far been implicated in colonial development. In cnidarians, colony ontogeny is characterized by the production of a nexus of vascular stolons, from which the feeding and reproductive structures, called polyps, are budded. Here we describe and characterize the Gsx parahox gene, Cnox-2, in the colonial cnidarian Hydractinia symbiolongicarpus of the class Hydrozoa. Cnox-2 is expressed in prominent components of the colony-wide patterning system; in the epithelia of distal stolon tips and polyp bud rudiments. Both are regions of active morphogenetic activity, characterized by cytologically and behaviorally distinct epithelia. Experimental induction and elimination of stolonal tips result in up- and down-regulation, respectively, of Cnox-2 expression. In the developing polyp, Cnox-2 expression remains uniformly high throughout the period of axial differentiation. The differential oral-aboral Cnox-2 expression in the epithelia of the mature polyp, previously described for this and another hydrozoan, arises after oral structures have completed development. Differential Cnox-2 expression is, thus, associated with key aspects of patterning of both the colony and the polyp, a finding that is particularly striking given that polyp and colony form are dissociable in the evolution of Hydrozoa.     

Polyp oriented modelling of coral growth

The morphogenesis of colonial stony corals is the result of the collective behaviour of many coral polyps depositing coral skeleton on top of the old skeleton on which they live. Yet, models of coral growth often consider the polyps as a single continuous surface. In the present work, the polyps are modelled individually. Each polyp takes up resources, deposits skeleton, buds off new polyps and dies. In this polyp oriented model, spontaneous branching occurs. We argue that branching is caused by a so called “polyp fanning effect” by which polyps on a convex surface have a competitive advantage relative to polyps on a flat or concave surface. The fanning effect generates a more potent branching mechanism than the Laplacian growth mechanism that we have studied previously (J. Theor. Biol. 224 (2003) 153). We discuss the application of the polyp oriented model to the study of environmentally driven morphological plasticity in stony corals. In a few examples we show how the properties of the individual polyps influence the whole colony morphology. In our model, the spacing of polyps influences the thickness of coral branches and the overall compactness of the colony. Density variations in the coral skeleton may also be important for the whole colony morphology, which we address by studying two variants of the model. Finally, we discuss the importance of small scale resource translocation in the coral colony and its effects on the morphology of the colony.     

Structure and signaling in polyps of a colonial hydroid

Abstract. After feeding, polyps of colonial hydroids contract regularly, dispersing food throughout the colony via the gastrovascular fluid. Such contractions may trigger signaling pathways that allow colonies to grow in an adaptive manner, i.e., to initiate development of more polyps in food‐rich areas and to suppress polyp development in food‐poor areas. In this context, we investigated the structure and potential signaling of the junction between polyps and stolons in colonies of the hydroid Podocoryna carnea. Using transmission electron microscopy, we found that the density of mitochondrion‐rich epitheliomuscular cells was low in polyp and stolon tissues except at or near the polyp‐stolon junction, where many of these mitochondrion‐rich cells occur in ectodermal tissue. In vivo fluorescence microscopy suggests that these mitochondria are a principal source of the metabolic signals of the colony. Both native fluorescence of NAD(P)H and fluorescence from peroxides (visualized with H₂DCFDA) co‐localize to this region of the polyp. Rhodamine 123 fluorescence suggests that both these metabolic signals emanate from mitochondria. To test whether such metabolic signals may be involved in colony pattern formation, inbred lines of P. carnea were used. Colonies of a runner‐like inbred line grow with widely spaced polyps and long stolonal connections, much like wild‐type colonies in a food‐poor environment. Colonies of a sheet‐like inbred line grow with closely spaced polyps and short stolonal connections, similar to wild‐type colonies in a food‐rich environment. Polyp‐stolon junctions in runner‐like and sheet‐like colonies were imaged for the fluorescence of H₂DCFDA. Densitometric analysis of this signal indicates that the mitochondria in epitheliomuscular cells of runner‐like polyps emit greater amounts of peroxides. Because peroxides and other reactive oxygen species are frequently intermediaries in metabolic signaling pathways, we suspect that such signaling may indeed occur at polyp‐stolon junctions, affecting colony pattern formation in these inbred lines and possibly in hydroid colonies in general.     

Self/non-self Discrimination in Basal Metazoa: Genetics of Allorecognition in the Hydroid Hydractinia

Colonial basal metazoans often encounter members of their ownspecies as they grow on hard substrata, with the encounterstypically resulting in either fusion of close relatives or rejectionbetween unrelated colonies. These allorecognition responsesplay a critical role in maintaining the genetic and physiologicalintegrity of the colony. Allorecognition responses in basalmetazoans are controlled by highly variable genetic systems.The molecular nature of such systems, however, remains to bedetermined. Current efforts to identify the genes and moleculescontrolling allorecognition in basal metazoans have followedtwo pathways: identification of molecules differentially expressedin incompatible interactions, and positional or map-based cloningof allorecognition genes. Most studies following the first approachhave been performed with marine demosponges, while those followingthe second approach have centered on the cnidarian of the genusHydractinia. Here, I discuss the latter, focusing primarilyon the genetic control of allorecognition responses.     

Molecular phylogenetics of the siphonophora (Cnidaria), with implications for the evolution of functional specialization

Siphonophores are a group of pelagic colonial hydrozoans (Cnidaria) that have long been of general interest because of the division of labor between the polyps and medusae that make up these "superorganisms." These polyps and medusae are each homologous to free living animals but are generated by an incomplete asexual budding process that leaves them physiologically integrated. They are functionally specialized for different tasks and are precisely organized within each colony. The number of functional types of polyps and medusae varies across taxa, and different authors have used this character to construct phylogenies polarized in opposite directions, depending on whether they thought siphonophore evolution proceeded by a reduction or an increase in functional specialization. We have collected taxa across all major groups of siphonophores, many of which are found exclusively in the deep sea, using remotely operated underwater vehicles (ROVs) and by SCUBA diving from ships in the open ocean. We have used 52 siphonophores and four outgroup taxa to estimate the siphonophore phylogeny with molecular data from the nuclear small subunit ribosomal RNA gene (18S) and the mitochondrial large subunit ribosomal RNA gene (16S). Parsimony reconstructions indicate that functionally specialized polyps and medusae have been gained and lost across the phylogeny. Maximum likelihood and Bayesian analyses of morphological data suggest that the transition rate for decreased functional specialization is greater than the transition rate for increased functional specialization for three out of the four investigated categories of polyps and medusae. The present analysis also bears on several long-standing questions about siphonophore systematics. It indicates that the cystonects are sister to all other siphonophores, a group that we call the Codonophora. We also find that the Calycophorae are nested within the Physonectae, and that the Brachystelia, a historically recognized grouping of short-stemmed taxa, are polyphyletic. [Cnidaria; colonial animals; deep sea; division of labor; functional specialization; Hydrozoa; phylogenetics; Siphonophores.].     

Another Origin of Coloniality in Volvocaleans: The Phylogenetic Position of Pyrobotrys Arnoldi (Spondylomoraceae,Volvocales)

ABSTRACT. Colonial volvocaleans (Chlorophyceae) are used as a standard model of multicellular evolution. However, the phylogenetic position of the colonial volvocalean family Spondylomoraceae has yet to be resolved. To examine this, the molecular phylogenies of Pyrobotrys stellata and Pyrobotrys squarrosa were analyzed using combined 18S rRNA, RUBISCO large subunit, and P700 chl a‐apoprotein A2 gene sequences. In the phylogenetic trees, Pyrobotrys belonged to the clade Caudivolvoxa and was not closely related to other colonial volvocalean flagellates. The results indicate that colony formation of Spondylomoraceae independently evolved from unicellular volvocaleans. The phylogenetic position of problematic “Pascherina tetras” SAG 159‐1 was also analyzed.     

A silent invasion

Invasions mediated by humans have been reported from around the world, and ships’ ballast water has been recognized as the main source of marine invaders worldwide. Some invasions have dramatic economic and ecological consequences. On the other hand, many invasions especially in the marine realm, can go unnoticed. Here we identify a human mediated, worldwide introduction of the hydrozoan species Turritopsis dohrnii. The normal life cycle of hydrozoans involves the asexual budding of medusae from colonial polyps. Medusae of Turritopsis, however, when starved or damaged, are able to revert their life cycle, going back to the polyp stage through a process called transdifferentiation. They can thus easily survive through long journeys in cargo ships and ballast waters. We have identified a clade of the mitochondrial 16S gene in Turritopsis which contains individuals collected from Japan, the Pacific and Atlantic coasts of Panama, Florida, Spain, and Italy differing from each other in only an average of 0.31% of their base-pairs. Fifteen individuals from Japan, Atlantic Panama, Spain, and Italy shared the same haplotype. Turritopsis dohrnii medusae, despite the lack of genetic differences, are morphologically different between the tropical and temperate locations we sampled, attesting to a process of phenotypic response to local conditions that contributes to making this grand scale invasion a silent one.     

Metamorphosis ofHydractinia echinata Insights into pattern formation in Hydroids

Summary Hydractinia echinata is a marine, colony-forming coelenterate. Fertilized eggs develop into freely swimming planula larvae, which undergo metamorphosis to a sessile (primary) polyp. Metamorphosis can be triggered by means of certain marine bacteria and by Cs⁺. Half a day after this treatment a larva will have developed into a polyp. The induction of metamorphosis can be prevented by addition of inhibitor I, a substance partially purified from tissue ofHydra. The larvae ofH. echinata also appear to contain this substance. Inhibitor I appliedafter the onset of metamorphosis blocks its continuation as long as it remains in the culture medium. Cs⁺ applied within the same period of time also blocks the continuation of metamorphosis. However, these two agents have opposite effects on the body pattern of the resultant polyps. The experiments indicate that application of Cs⁺ triggers the generation of the pre-pattern. Inhibitor I appears to be a factor of this prepattern. A model is proposed which describes the basic features of head and foot/stolon formation not only forHydractinia but also for other related hydroids.