The hydroid fossil record and analytical techniques for assessing the affinities of putative hydrozoans and possible hemichordates

Hydrozoan cnidarians are widespread in modern environments, but their polyps or hydroids, when not biomineralized, are generally rare in the fossil record. To assess the affinities of four hydrozoan taxa previously described on the basis of supposed fossils of non‐biomineralized hydroids, we re‐analysed the type specimens of these taxa using a combination of light and electron microscopic tools, including backscattered electron (BSE) scanning electron microscopy (SEM) and energy‐dispersive X‐ray spectroscopy (EDS). New morphological, ultrastructural and taphonomic data were generated for Archaeoantennularia byersi from the Devonian of Michigan, Archaeocryptolaria compacta from the Ordovician of Virginia, and Mazohydra megabertha and Drevotella proteana from the Carboniferous Mazon Creek Lagerstätte of Illinois, which are preserved as carbonaceous fossils, aluminosilicate films and iron carbonate minerals in siderite concretions, respectively. In the context of these results, we provide a review of the fossil record of non‐biomineralized hydroids, describe possible biases and changes through time in their occurrence and preservation, and evaluate the criteria commonly used to identify and interpret their fossils. Although hydroids have been reported from Phanerozoic (particularly lower Palaeozoic) rocks around the world, many putative hydroids from the Palaeozoic are poorly substantiated and may actually be hemichordates. Indeed, none of the type specimens in this study represent unequivocal hydrozoans. As shown in BSE images, metatype specimens of A. byersi possess autothecae, fusellae, stolons, stolothecae and bithecae, which decisively indicate that they are dendroid graptolites rather than hydroids. The analyses yielded no evidence that A. compacta, Mazohydra and Drevotella are hydrozoans, as their holotypes lack the diagnostic morphological, taphonomic and ecological features characteristic of purported hydroid analogues. Consequently, our results suggest that many Palaeozoic hydroids may be hemichordates and that interpretations of hydroid fossils should be tested and refined using data collected via in situ analytical techniques like BSE‐SEM and EDS.     

Probable advanced hydroid from the Early Ordovician of China

A fossil of a colonial organism with pyritized soft tissues of elongated fusiform zooids, found in the middle part of the early Floian Fenxiang Formation in Hubei Province of China, probably represents the oldest reliable record of a hydroid cnidarian. The preservation of the fossil is sufficiently different from that of associated carbonized skeletons of graptolites to exclude affinities with this group. The fossil is unlikely to be a bryozoan because of the mode of budding from proximal, not distal, parts of parent zooids, which is typical rather of hydroids. Although no thecae are preserved, the fossil, named Sinobryon elongatum gen. et sp. nov., is suggested to be a thecate hydroid, possibly related to the Haleciidae. The apparent presence of an advanced member of the thecaphoran Macrocolonia clade in strata 470 Ma old means that much of the hydroid (and cnidarian) diversification preceded the Middle Ordovician.     

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.     

Induction of reverse development in two marine Hydrozoans

Cnidarians are unique organisms in the animal kingdom because of their unequalled potential to undergo reverse development (RD). The life cycle of some species can temporarily shift ordinary, downstream development from zygote to adult into the opposite ontogenetic direction by back-transformation of some life stages. The potential for RD in cnidarians offers the possibility to investigate how integrative signalling networks operate to control directionality of ontogeny (reverse vs. normal development). Striking examples are found in some hydrozoans, where RD of medusa bud or liberated medusa stages leads to rejuvenation of the post-larval polyp stage. Artificial stress may determine ontogeny reversal. We describe here the results of experimental assays on artificial induction of RD by different chemical and physical inducers on two marine hydrozoans, Turritopsis dohrnii and Hydractinia carnea, showing a different potential for RD. A cascade of morphogenetic events occurs during RD by molecular mechanisms and cellular patterns recalling larval metamorphosis. For the first time, we show here that exposure to cesium chloride (CsCl), an inducer of larval metamorphosis, may also induce RD, highlighting similarities and differences between these two master ontogenetic processes in cnidarians.     

nanos expression at the embryonic posterior pole and the medusa phase in the hydrozoan Podocoryne carnea

Summary The distinction between soma and germline is an important process in the development of animals with sexual reproduction. It is regulated by a number of germline-specific genes, most of which appear conserved in evolution and therefore can be used to study the formation of the germline in diverged animal groups. Here we report the isolation of two orthologs of one such gene, nanos (nos), in the cnidarian Podocoryne carnea, a species with representative zoological features among the hydrozoans. By studying nos gene expression throughout the Podocoryne biphasic life cycle, we find that the germline differentiates exclusively during medusa development, whereas the polyp does not contribute to the process. An early widespread nos expression in developing medusae progressively refines into a mainly germline-specific pattern at terminal stages of medusa formation. Thus, the distinction between germline and soma is a late event in hydrozoan development. Also, we show that the formation of the medusa is a de novo process that relies on active local cell proliferation and differentiation of novel cell and tissue types not present in the polyp, including nos-expressing cells. Finally, we find nos expression at the posterior pole of Podocoryne developing embryos, not related to germline formation. This second aspect of nos expression is also found in Drosophila, where nos functions as a posterior determinant essential for the formation of the fly abdomen. This raises the possibility that nos embryonic expression could play a role in establishing axial polarity in cnidarians.     

Hydroid epifaunal communities in Arctic coastal waters (Svalbard): effects of substrate characteristics

The knowledge of cryptic epifaunal groups in the Arctic is far from complete mostly due to logistic difficulties. Only recently, advances in sample collection using SCUBA diving techniques have enabled to explore delicate hydroid fauna from shallow waters. This study is the first attempt to examine the relationship between substrate property (such as size of rock, morphological characteristics of algal or bryozoan host) and hydroid community composition and diversity in the Arctic. Samples of substrates for hydroid attachment including rocks, algae, bryozoans and other hydrozoans were collected around the Svalbard. Examination revealed no substrate-specific species. The substrate property did not have a strong influence on hydroid community. Both species composition and richness were not related to colonized rock surface area and to morphological characteristic of algal host. Therefore, results indicate the opportunistic nature of hydroid fauna in terms of substrate preference. However, the presence or absence of hydroids depended on the surface area of rocky substrate. Hydroids were more often present on rocks of larger surface area. Erect hydroids and bryozoans were important attachment surface for stolonal hydroids.     

The life cycle of Hydrichthys tnirus (Gnidaria: Hydrozoa: Anthomedusae: Pandeidae)

The previously unknown life cycle of the parasitic hydroid Hydrichthys mirus is described. The adult medusa has 5–6 tentacles and could be referred to Leuckartiara. Another species of Hydrichthys has previously been shown to have a Stomotoca -like medusa, characterized by the possession of two tentacles. It is proposed that Hydrichthys originated from the Leuckartiara lineage and that, through paedomorphosis in at least one species, the medusa retained the two-tentacle state of the newly-released medusa of all pandeids, thus becoming referable to Stomotoca. It is suggested that Stomotoca has hitherto constituted a polyphyletic taxon, embracing parallel lineages of pandeids, each retaining juvenile features. An additional genus, Larsonia , is introduced to accommodate species with Stomotoca-like medusae and Hydrichthys -like hydroids.     

A new hydroid from the Upper Cretaceous of Mississippi

A new fossil hydroid is reported as an organic impression on a calcareous gastropod steinkern from the Prairie Bluff Chalk (Maastrichtian), Oktibbeha County, Mississippi. This is the first such hydroid reported from the Upper Cretaceous of the Atlantic Coastal Plain. The fossil organism consists of anastomosing hydrorhizae forming a holdfast, a fascicled hydrocaulus, and elongated, crenulated and ribbed hydrothecae. The fossil is unlike other Mesozoic hydroids that have been reported from Europe and North America; it is described as Mesodendrium oktibbehaensis gen. et sp. nov. and tentiatively referred to an extant family, the Campanulariidae (Calyptoblastina). The complete preservation of the holdfast, hydrocaulus and hydrothecae suggests that this hydroid lived inside gastropod shells. In analogy with Recent symbiotic hydroids inhabiting mollusc shells, the new specimen described here possibly represents the oldest known example of a symbiotic relationship between hydroids and hermit crabs.     

Convergent origins and rapid evolution of spliced leader trans-splicing in Metazoa: Insights from the Ctenophora and Hydrozoa

Replacement of mRNA 5′ UTR sequences by short sequences trans-spliced from specialized, noncoding, spliced leader (SL) RNAs is an enigmatic phenomenon, occurring in a set of distantly related animal groups including urochordates, nematodes, flatworms, and hydra, as well as in Euglenozoa and dinoflagellates. Whether SL trans-splicing has a common evolutionary origin and biological function among different organisms remains unclear. We have undertaken a systematic identification of SL exons in cDNA sequence data sets from non-bilaterian metazoan species and their closest unicellular relatives. SL exons were identified in ctenophores and in hydrozoan cnidarians, but not in other cnidarians, placozoans, or sponges, or in animal unicellular relatives. Mapping of SL absence/presence obtained from this and previous studies onto current phylogenetic trees favors an evolutionary scenario involving multiple origins for SLs during eumetazoan evolution rather than loss from a common ancestor. In both ctenophore and hydrozoan species, multiple SL sequences were identified, showing high sequence diversity. Detailed analysis of a large data set generated for the hydrozoan Clytia hemisphaerica revealed trans-splicing of given mRNAs by multiple alternative SLs. No evidence was found for a common identity of trans-spliced mRNAs between different hydrozoans. One feature found specifically to characterize SL-spliced mRNAs in hydrozoans, however, was a marked adenosine enrichment immediately 3′ of the SL acceptor splice site. Our findings of high sequence divergence and apparently indiscriminate use of SLs in hydrozoans, along with recent findings in other taxa, indicate that SL genes have evolved rapidly in parallel in diverse animal groups, with constraint on SL exon sequence evolution being apparently rare.     

Telomerase activity is not related to life history stage in the jellyfish Cassiopea sp.

The polyp (scyphistoma) of the jellyfish Cassiopea sp. can be maintained in culture for a long time, as polyps repeatedly reproduce asexually via formation of vegetative buds or propagules. The medusa, which is the sexually reproducing stage, typically has a relatively short life span. As a first step to understand the difference in life spans of the polyp and medusa stages of Cassiopea sp., we measured telomerase activity in different life cycle stages. We found telomerase activity in tissues of aposymbiotic polyps and propagules and symbiotic ephyrae (newly budded medusae) and adult medusae. No significant difference in telomerase activity was found between polyps and the bell region of the medusae. The cloned elongation products of the stretch PCR contained the TTAGGG repeats suggesting that the jellyfish has the ‘vertebrate’ telomere motif (TTAGGG)_n. This is the first study to show that somatic tissues of both polyp and medusa stages of a cnidarian had telomerase activity. Telomerase activity in somatic tissues may be related to the presence of multipotent interstitial cells and high regenerative capacity of cnidarians.     

Cnidarian taphonomy and affinities of the Ediacara biota

Plaster impressions and sand casts of extant medusae, a chondrophoran, and a pennatulid share basic structural characteristics with fossils in the Upper Proterozoic Ediacara assemblage. Impressions of extant medusae and Proterozoic circular impressions show general similarities in arrangement and position of radial and concentric structures and a central raised boss. However, annular rings and radial grooves are more numerous in the Proterozoic fossils and strongly folded or deformed fossils are rare as compared with impressions of modem medusae. Recent pennatulids yield impressions that are more deformed and irregular than the Proterozoic genus Charniodiscus. The greater frequency of deformation of most simulated fossil medusoids relative to Precambrian circular impressions implies that Proterozoic medu-soids were substantially stiffer than many modern taxa of comparable sizes. Many fossils with abundant circular rings have no constructional counterparts among the extant forms studied here and their medusoid affinities should remain in doubt. The structural simplicity of impressions of Ediacara organisms and extant cnidarians suggests that their mutual similarities may be due to convergence. However, there is no compelling morphological reason to reject the claim that some Proterozoic fossils may share affinities with living cnidarians. □ Taphonomy. Ediacara biota, cnidarians, phylogenetic relationships.     

Feeding strategies and diet composition of four Antarctic cnidarian species

The diet of four species of Antarctic cnidarians, two hydroids and two anthozoans, was investigated. One hydroid, Tubularia ralphii, and one anthozoan, Anthomastus bathyproctus, seem to basically consume zooplankton whereas the other hydroid species, Oswaldella antarctica, has a diet mainly based on the fine fraction of seston. The last cnidarian investigated, the stoloniferan alcyonacean, Clavularia cf. frankliniana, feeds mainly on resuspended material. The wide range of diets of these Antarctic cnidarians indicates opportunistic behaviour by feeding on different sources and taking advantage of the available food sources. Data related to low C/N ratios in the sediment and high NO₂ concentrations in areas with dense communities of benthic suspension feeders, along with data on capture rates, lead us to hypothesize that these organisms play an important role in the recycling processes of organic matter in Antarctic benthic ecosystems.     

The evolution of the immune-type gene family Rhamnospondin in cnidarians

Rhamnose-binding lectins (RBLs) in vertebrates function in immunity as pattern recognition receptors, opsonization agents, and activators of pro-inflammatory cytokines. Although they have been identified in some invertebrate taxa, their distribution, function, and evolutionary patterns in basal metazoans, remain largely unknown. A unique RBL-containing protein composed of 8 thrombospondin type 1 repeats (TSRs) and a single RBL domain has been identified in the colonial hydroid Hydractinia symbiolongicarpus. This Rhamnospondin (Rsp) gene was specifically and constitutively expressed in the mouth of feeding polyps. Here we report the full characterization of a second Rsp gene from a H. symbiolongicarpus BAC library. Rsp1 and Rsp2 were 1.1kb apart, shared the same domain architecture and were 93% identical. Introns differed substantially in size and sequence, excepting two introns that were nearly identical, suggesting the action of inter-locus recombination. Sequencing full-length cDNAs from a wild-type individual corroborated the exon boundaries predicted from genomic DNA and showed gene polymorphism at both loci. Database searches and phylogenetic analyses showed that Rsp was found only in hydrozoans, indicating that it is an innovation of the cnidarian class Hydrozoa. Phylogenetic analysis of Rsp sequences in hydroids show a tendency of clustering paralogous genes, suggesting that they have evolved by concerted evolution.     

Novel conducting tissues in Lower Devonian plants

Elongate cells presumed to comprise water-conducting tissues are described from the central regions of short lengths of two naked, stomatiferous, coalified, axial fossils from Lochkovian (Lower Devonian) fluvial rocks in the Welsh Borderland. In one, a discrete central strand is predominantly composed of uniformly thickened cells that are compared with central tissues in coeval plants, e.g. Aglaophyton , and the hydroids of extant mosses. The other has at least two types of cells with pits of plasmodesmata dimensions that perforate only the inner layer of a bilayered wall. These are compared with liverwort and Takakia hydroids and the coeval S-type tracheids that characterize the Rhyniopsida. The affinities of the two axes remain equivocal. The relevance of plasmodesmata-derived pits to the evolution of diversity in water-conducting elements in early cmbryophytes is discussed.     

Polypengeneration und Entwicklungsgeschichte vonEucheilota maculata (Thecata-Leptomedusae)

Polyps and medusae differ in regard to habitats, evolution, and morphological structures. In order to replace the former taxonomic systems which deal with polyp and medusa generations separately, by a single valid classification including both generations, knowledge of all essential life history phases is necessary. Modern methods of culturing marine hydroids are outlined briefly. Successful culturing provides the means to link formerly unidentified polyps or medusae with one another. The present paper is concerned with the hydroidEucheilota maculata Hartlaub, the medusa of which is common in the southern North Sea. The polyps formerly unknown have been reared from fertilized eggs of the medusae. They were raised to full size, formed colonies, and produced gonangia and medusae. Thus the morphology of the single polyp, the polyp colony, and of the young medusa could be investigated in detail. The nematocyst equipment of the two generations and of all developmental stages is described as well as the number of chromosomes. The systematic position of the genusEucheilota is discussed and the diagnosis of the speciesE. maculata, including the two generations, given.     

Green Fluorescence of Cytaeis Hydroids Living in Association with Nassarius Gastropods in the Red Sea

Green Fluorescent Proteins (GFPs) have been reported from a wide diversity of medusae, but only a few observations of green fluorescence have been reported for hydroid colonies. In this study, we report on fluorescence displayed by hydroid polyps of the genus Cytaeis Eschscholtz, 1829 (Hydrozoa: Anthoathecata: Filifera) found at night time in the southern Red Sea (Saudi Arabia) living on shells of the gastropod Nassarius margaritifer (Dunker, 1847) (Neogastropoda: Buccinoidea: Nassariidae). We examined the fluorescence of these polyps and compare with previously reported data. Intensive green fluorescence with a spectral peak at 518 nm was detected in the hypostome of the Cytaeis polyps, unlike in previous reports that reported fluorescence either in the basal parts of polyps or in other locations on hydroid colonies. These results suggest that fluorescence may be widespread not only in medusae, but also in polyps, and also suggests that the patterns of fluorescence localization can vary in closely related species. The fluorescence of polyps may be potentially useful for field identification of cryptic species and study of geographical distributions of such hydroids and their hosts.     

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.     

KIN INTERACTIONS IN A COLONIAL HYDROZOAN (HYDRACTINIA SYMBIOLONGICARPUS): POPULATION STRUCTURE ON A MOBILE LANDSCAPE

Many sessile colonial organisms intensively compete with conspecifics for growing space. This competition can result in either cooperative fusion or aggressive rejection between colonies, and some species have evolved highly polymorphic genetic systems that mediate the outcome of these interactions. Here we demonstrate the potential for interactions among close kin as the basis for the evolutionary maintenance of a genetically polymorphic allorecognition system in the colonial hydroid Hydractinia symbiolongicarpus, which lives on gastropod shells occupied by hermit crabs. Fusion between hydroids in the laboratory is restricted mainly to encounters between full siblings, whereas other encounters result in aggressive rejection. Natural selection acting on the costs or benefits of fusion between colonies could be responsible for the present maintenance of such a highly specific behavioral response, but only if encounters between fusible colonies still occur in contemporary populations. The large size of these hydroid populations and the mobility of the crabs should limit the potential for interactions among closely related hydroids on the same shell. However, RAPD polymorphisms among a large sample of hydroids from a population off the coast of Massachusetts indicate that genetically similar colonies are often found together on the same shell. Some genetic distances between colonies on the same shell were low relative to genetic distances between colonies on different shells or genetic distances between known full siblings from laboratory matings. We conservatively estimate that 2–18% of co-occurring colonies may be full sibling pairs. These observations suggest that encounters between genetically similar hydroids are common, despite the mobile nature of their habitat, and these encounters may provide frequent opportunities for natural selection to influence the evolution of cooperative and agonistic behaviors and their polymorphic genetic basis.     

埃迪卡拉纪至寒武纪苗岭世刺细胞动物化石研究现状与展望

刺细胞动物是一类具有刺细胞的水生无脊椎动物,分布在世界各地的海洋和淡水中。作为后生动物最早分化出的一支,刺细胞动物对研究后生动物的起源和早期演化具有极其重要的意义,也为研究后生动物系统发育、地层对比和古地理恢复等方面提供了重要的科研线索。本文简要介绍了刺细胞动物早期(埃迪卡拉纪至寒武纪苗岭世)的化石记录和研究现状,将刺细胞动物的早期演化分为四个时期,分别为前寒武纪、寒武纪纽芬兰世、寒武纪第二世和寒武纪苗岭世,并对上述四个时期的刺细胞动物进行论述。目前的研究表明:1)前寒武纪的刺细胞动物化石记录虽然比较丰富,但充满争议,目前尚未有比较确切的刺细胞动物记录;2)寒武纪纽芬兰世如宽川铺生物群中保存了较多的刺细胞动物胚胎及发育序列化石,是研究刺细胞动物演化的重要窗口;3)寒武纪第二世,以澄江生物群为代表的布尔吉斯页岩型化石保存了软躯体的刺细胞动物。与此同时,在第二世中已经出现了最早的珊瑚化石记录;4)寒武纪苗岭世刺细胞动物主要以布尔吉斯页岩型化石保存(如布尔吉斯页岩生物群和凯里生物群),同时期在美国犹他州发现的刺细胞动物印痕化石表明了这个时期几乎所有的刺细胞动物大类已经出现。本文根据上述时期的研究,对今后刺细胞动物化石的研究提供一些建议和讨论。