Cladistic analysis of Medusozoa and cnidarian evolution

Abstract. A cladistic analysis of 87 morphological and life history characters of medusozoan cnidarians, rooted with Anthozoa, results in the phylogenetic hypothesis (Anthozoa (Hydrozoa (Scyphozoa (Staurozoa, Cubozoa)))). Staurozoa is a new class of Cnidaria consisting of Stauromedusae and the fossil group Conulatae. Scyphozoa is redefined as including those medusozoans characterized by strobilation and ephyrae (Coronatae, Semaeostomeae, and Rhizostomeae). Within Hydrozoa, Limnomedusae is identified as either the earliest diverging hydrozoan lineage or as the basal group of either Trachylina (Actinulida (Trachymedusae (Narcomedusae, Laingiomedusae))) or Hydroidolina (Leptothecata (Siphonophorae, Anthoathecata)). Cladistic results are highly congruent with recently published phylogenetic analyses based on 18S molecular characters. We propose a phylogenetic classification of Medusozoa that is consistent with phylogenetic hypotheses based on our cladistic results, as well as those derived from 18S analyses. Optimization of the characters presented in this analysis are used to discuss evolutionary scenarios. The ancestral cnidarian probably had a sessile biradial polyp as an adult form. The medusa is inferred to be a synapomorphy of Medusozoa. However, the ancestral process (metamorphosis of the apical region of the polyp or lateral budding involving an entocodon) could not be inferred unequivocally. Similarly, character states for sense organs and nervous systems could not be inferred for the ancestral medusoid of Medusozoa.     

Phylogenetic analysis of the Cnidaria

The recent members of the phylum Cnidaria were analyzed with phylogenetic methodology and the help of the PAUP Computer program. The Cnidaria are established as a monophylum by their cnidocysts, planula larva, and a polyp stage. The Ctenophora were seen as the most probable sister group of the Cnidaria. Arguments for the monophyly of the cnidarian classes Anthozoa, Scyphozoa, Cubozoa, and Hydrozoa were providea. For the ground plan of the Cnidaria the following characters were postulated: triphasic life cycle consisting of a planula larva, a benthic polyp stage, and a sexually propagating medusa like stage. For the polyp a radial symmetry, lack of septae, and hollow tentacles were assumed. The original medusa probably was tetraradial and developed from the polyp stage by a total metamorphosis. Twelve polarized characters were used to generate cladograms. The most parsimonious one showed the Anthozoa as the first offshoot of the tree with the united Scyphozoa, Cubozoa and Hydrozoa forming its sister group. Within this sister group the Scyphozoa and Cubozoa were seen as sistergroups to each other. Both groups united are then the sistergroup of the Hydrozoa. A bootstrap analysis yielded the same tree with high probabilities for the internal nodes. Despite assuming a planktonic origin of the Cnidaria in this investigation, the resulting cladogram is also compatible with an evolution of the medusa stage within the Cnidaria after the splitting-off of the Anthozoa. The possible loss of the medusa stage in the Anthozoa is discussed.     

Phylogeny of Medusozoa and the evolution of cnidarian life cycles

To investigate the evolution of cnidarian life cycles, data from the small subunit of the ribosome are used to derive a phylogenetic hypothesis for Medusozoa. These data indicate that Cnidaria is monophyletic and composed of Anthozoa and Medusozoa. While Cubozoa and Hydrozoa are well supported clades, Scyphozoa appears to be paraphyletic. Stauromedusae is possibly the sister group of either Cubozoa or all other medusozoans. The phylogenetic results suggest that: the polyp probably preceded the medusa in the evolution of Cnidaria; within Hydrozoa, medusa development involving the entocodon is ancestral; within Trachylina, the polyp was lost and subsequently regained in the parasitic narcomedusans; within Siphonophorae, the float originated prior to swimming bells; stauromedusans are not likely to be descended from ancestors that produced medusae by strobilation; and cubozoan polyps are simplified from those of their ancestors, which possessed polyps with gastric septa and four mesogleal muscle bands and peristomial pits.     

Monophyly of Anthozoa (Cnidaria): why do nuclear and mitochondrial phylogenies disagree?

The phylum Cnidaria is usually divided into five classes: Anthozoa, Cubozoa, Hydrozoa, Scyphozoa and Staurozoa. The class Anthozoa is subdivided into two subclasses: Hexacorallia and Octocorallia. Morphological and molecular studies based on nuclear rDNA and recent phylogenomic studies support the monophyly of Anthozoa. On the other hand, molecular studies based on mitochondrial markers, including two recent studies based on mitogenomic data, supported the paraphyly of Anthozoa, and positioned Octocorallia as sister group to Medusozoa (the monophyletic group of Cubozoa, Hydrozoa and Scyphozoa). On the basis of 51 nuclear orthologs from four hexacorallians, four octocorallians, two hydrozoans and one scyphozoan (with poriferans and Homo sapiens as out‐groups), we built a multilocus alignment of 9 873 amino acids, which aimed at minimizing missing data and hidden paralogy, in order to understand the discrepancy between nuclear and mitochondrial phylogenies. Our phylogenetic analyses strongly supported the monophyly of Anthozoa. We compared the level of substitution saturation between our data set, the data sets of two recent phylogenomic studies and one of a mitogenomic study. We found that mitochondrial DNA is more saturated than nuclear DNA at all the phylogenetic levels studied. Our results emphasize the need for a good evaluation of phylogenetic signal.     

Ontogeny and homology of the claustra in otophysan Ostariophysi (Teleostei)

We studied the ontogeny of the claustrum comparatively in representatives of all otophysan subgroups. The claustrum of cypriniforms has a cartilaginous precursor, the claustral cartilage, which subsequently ossifies perichondrally at its anterior face and develops an extensive lamina of membrane bone. The membrane bone component of the claustrum and its close association with the atrium sinus imparis, a perilymphatic space of the Weberian apparatus, are both synapomorphies of cypriniforms. The characiform claustrum is not preformed in cartilage and originates as a membrane bone ossification, a putative synapomorphy of that taxon. Among siluriforms, the claustrum is present only in more basal groups and originates as an elongate cartilage that ossifies in a characteristic ventrodorsal direction, possibly a synapomorphy of catfishes. Gymnotiforms lack the claustral cartilage and claustrum. We review all previous hypothesis of claustrum homology in light of the above findings and conclude that the most plausible hypothesis is the one originally proposed by Bloch ([1900] Jen Z Naturw 34:1-64) that claustra are homologs of the supradorsals of the first vertebra.     

Some implications of molecular phylogenetics for understanding biodiversity in jellyfishes,with emphasis on Scyphozoa

Statistical phylogenetic analyses of 111 5.8S and partial-28S ribosomal DNA sequences (total aligned length=434 nucleotides) including jellyfishes representing approximately 14 of known scyphozoan morphospecies (21 genera, 62 families, and 100 orders) are presented. These analyses indicate stauromedusae constitute a fifth cnidarian class (Staurozoa) basal to a monophyletic Medusozoa (=Cubozoa, Hydrozoa, and Scyphozoa). Phylogenetic relationships among the medusozoans are generally poorly resolved, but support is found for reciprocal monophyly of the Cubozoa, Hydrozoa, Coronatae, and Discomedusae (=Semaeostomeae + Rhizostomeae). In addition, a survey of pairwise sequence differences in Internal Transcribed Spacer One within morphospecies indicates that scyphozoan species diversity may be approximately twice recent estimates based on morphological analyses. These results highlight difficulties with traditional morphological treatments including terminology that obfuscates homologies. By integrating molecular phylogenetic analyses with old and new morphological, behavioural, developmental, physiological, and other data, a much richer understanding of the biodiversity and evolution of jellyfishes is achievable.     

Somatostatin signaling system as an ancestral mechanism: Myoregulatory activity of an Allatostatin-C peptide in Hydra

The coordination of physiological processes requires precise communication between cells. Cellular interactions allow cells to be functionally related, facilitating the maintaining of homeostasis. Neuropeptides functioning as intercellular signals are widely distributed in Metazoa. It is assumed that neuropeptides were the first intercellular transmitters, appearing early during the evolution. In Cnidarians, neuropeptides are mainly involved in neurotransmission, acting directly or indirectly on epithelial muscle cells, and thereby controlling coordinated movements. Allatostatins are a group of chemically unrelated neuropeptides that were originally characterized based on their ability to inhibit juvenil hormone synthesis in insects. Allatostatin-C has pleiotropic functions, acting as myoregulator in several insects. In these studies, we analyzed the myoregulatory effect of Aedes aegypti Allatostatin-C in Hydra sp., a member of the phylum Cnidaria. Allatostatin-C peptide conjugated with Qdots revealed specifically distributed cell populations that respond to the peptide in different regions of hydroids. In vivo physiological assays using Allatostatin-C showed that the peptide induced changes in shape and length in tentacles, peduncle and gastrovascular cavity. The observed changes were dose and time dependent suggesting the physiological nature of the response. Furthermore, at highest doses, Allatostatin-C induced peristaltic movements of the gastrovascular cavity resembling those that occur during feeding. In silico search of putative Allatostatin-C receptors in Cnidaria showed that genomes predict the existence of proteins of the somatostatin/Allatostatin-C receptors family. Altogether, these results suggest that Allatostatin-C has myoregulatory activity in Hydra sp, playing a role in the control of coordinated movements during feeding, indicating that Allatostatin-C/Somatostatin based signaling might be an ancestral mechanism.     

Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models

A newly compiled data set of nearly complete sequences of the large subunit of the nuclear ribosome (LSU or 28S) sampled from 31 diverse medusozoans greatly clarifies the phylogenetic history of Cnidaria. These data have substantial power to discern among many of the competing hypotheses of relationship derived from prior work. Moreover, LSU data provide strong support at key nodes that were equivocal based on other molecular markers. Combining LSU sequences with those of the small subunit of the nuclear ribosome (SSU or 18S), we present a detailed working hypothesis of medusozoan relationships and discuss character evolution within this diverse clade. Stauromedusae, comprising the benthic, so-called stalked jellyfish, appears to be the sister group of all other medusozoans, implying that the free-swimming medusa stage, the motor nerve net, and statocysts of ecto-endodermal origin are features derived within Medusozoa. Cubozoans, which have had uncertain phylogenetic affinities since the elucidation of their life cycles, form a clade-named Acraspeda-with the scyphozoan groups Coronatae, Rhizostomeae, and Semaeostomeae. The polyps of both cubozoans and hydrozoans appear to be secondarily simplified. Hydrozoa is comprised by two well-supported clades, Trachylina and Hydroidolina. The position of Limnomedusae within Trachylina indicates that the ancestral hydrozoan had a biphasic life cycle and that the medusa was formed via an entocodon. Recently hypothesized homologies between the entocodon and bilaterian mesoderm are therefore suspect. Laingiomedusae, which has often been viewed as a close ally of the trachyline group Narcomedusae, is instead shown to be unambiguously a member of Hydroidolina. The important model organisms of the Hydra species complex are part of a clade, Aplanulata, with other hydrozoans possessing direct development not involving a ciliated planula stage. Finally, applying phylogenetic mixture models to our data proved to be of little additional value over a more traditional phylogenetic approach involving explicit hypothesis testing and bootstrap analyses under multiple optimality criteria. [18S; 28S; Cubozoa; Hydrozoa; medusa; molecular systematics; polyp; Scyphozoa; Staurozoa.].     

Anatomy and affinities of a new 535‐million‐year‐old medusozoan from the Kuanchuanpu Formation,South China

We describe here Sinaster petalon gen. et sp. nov., a new embryonic form from the c. 535 million‐year‐old Kuanchuanpu Formation of South China (Ningqiang, Shaanxi Province). The excellent three‐dimensional, phosphatic preservation of these microfossils allowed us to use x‐ray microtomographic techniques to make accurate reconstructions of their internal structures and to compare their anatomy point‐by‐point with that of extant cnidarians and other animal groups. Sinaster petalon has anatomical features typical of extant Medusozoa (Cnidaria), such as coronal muscles, perradial and adradial frenula, interradial septa, accessory septa, gonad‐lamellae, tentacle buds and perradial pockets. Although Sinaster cannot be straightforwardly assigned to any crown‐group within Medusozoa, the presence of marginal lappets and endodermal lamellae suggests that it is closer to Cubozoa and Scyphozoa than to any other group of modern cnidarians. The tentative placement of Sinaster within the stem‐group Cubozoa is justified by the presence of a velarium supported by a frenulum. The cubozoan affinities of Sinaster are also supported by cladistic analysis.     

An evolutionary comparative analysis of the medusozoan (Cnidaria) exoskeleton

The benthic polyp phase of Medusozoa (Staurozoa, Cubozoa, Scyphozoa, and Hydrozoa) has endoskeletal or exoskeletal support systems, but their composition, development, and evolution is poorly known. In this contribution the variation in synthesis, structure, and function of the medusozoan exoskeleton was examined. In addition, an evolutionary hypothesis for its origin and diversification is proposed for both extinct and extant medusozoans. We also critically reviewed the literature and included data from our own histological and microstructural analyses of some groups. Chitin is a characteristic component of exoskeleton in Medusozoa, functioning as support, protection, and a reserve for various ions and inorganic and organic molecules, which may persuade biomineralization, resulting in rigid biomineralized exoskeletons. Skeletogenesis in Medusozoa dates back to the Ediacaran, when potentially synergetic biotic, abiotic, and physiological processes resulted in development of rigid structures that became the exoskeleton. Of the many types of exoskeletons that evolved, the corneous (chitin‐protein) exoskeleton predominates today in polyps of medusozoans, with its greatest variation and complexity in the polyps of Hydroidolina. A new type of bilayered exoskeleton in which there is an exosarc complementing the perisarc construction is here described.     

Evolutionary origin of rhopalia: insights from cellular‐level analyses of Otx and POU expression patterns in the developing rhopalial nervous system

SUMMARY In Cnidaria, the medusae of Scyphozoa and its sister‐group Cubozoa uniquely possess rhopalia at their bell margin. These sensory centers coordinate behavior and development. We used fluorescent in situ hybridization and confocal microscopy to examine mRNA expression patterns in Aurelia sp.1 (Cnidaria, Scyphozoa) during early medusa formation, while simultaneously visualizing the developing nervous system by immunofluorescence. The genes investigated include AurOtx1, and the POU genes, AurPit1, and AurBrn3, homologs of genes known to function in cephalar neural organization and sensory cell differentiation across Bilateria. Our results show that AurOtx1 expression defines the major part of the oral neuroectodermal domain of the rhopalium, within which distinct populations of AurBrn3‐ and AurPit1‐expressing sensory cells develop. Thus, despite the unique attributes of rhopalial evolution, we suggest that the rhopalial nervous system of scyphozoan medusae involves similar patterns of differential expression of genes that function in bilaterian cephalic structure and neuroendocrine system development. We propose that rhopalia evolved from preexisting sensory structures that developed distinct populations of sensory cells differentially expressing POU genes within Otx oral‐neuroectodermal domains. This implies some commonality of developmental genetic functions involving these genes in the still poorly constrained common ancestor of bilaterians and cnidarians.     

The early ANTP gene repertoire: insights from the placozoan genome

The evolution of ANTP genes in the Metazoa has been the subject of conflicting hypotheses derived from full or partial gene sequences and genomic organization in higher animals. Whole genome sequences have recently filled in some crucial gaps for the basal metazoan phyla Cnidaria and Porifera. Here we analyze the complete genome of Trichoplax adhaerens, representing the basal metazoan phylum Placozoa, for its set of ANTP class genes. The Trichoplax genome encodes representatives of Hox/ParaHox-like, NKL, and extended Hox genes. This repertoire possibly mirrors the condition of a hypothetical cnidarian-bilaterian ancestor. The evolution of the cnidarian and bilaterian ANTP gene repertoires can be deduced by a limited number of cis-duplications of NKL and "extended Hox" genes and the presence of a single ancestral "ProtoHox" gene.     

Visual ecology and functional morphology of cubozoa (cnidaria)

Jellyfish belong to one of the oldest extant animal phyla, the Cnidaria. The first Cnidaria appear in the fossil record 600 million years ago, preceeding the Cambrian explosion. They are an extremely successful group present in all marine environments and some freshwater environments. In contrast to many animal phyla in which vision is a primary sense Cnidarians do not, generally, employ image forming eyes. One small class stands alone: the Cubozoa. Cubomedusae are commonly known as box jellyfish. They possess image forming eyes (Coates et al., 2001) which certainly evolved independently from other metazoans. Cubomedusae therefore offer a unique perspective on the evolution of image forming eyes. This literature review collects, into one place, what is known about: the multiple eye types of box jellyfish, cubomedusan life history and ecology, and the sensory and neural systems of box jellyfish. Here I discuss how these features set cubomedusae apart from scyphomedusae and hydromedusae. Knowledge in these areas is sparse; the work done to date inspires increased efforts.     

What is the function of the claustrum?

The claustrum is a thin, irregular, sheet-like neuronal structure hidden beneath the inner surface of the neocortex in the general region of the insula. Its function is enigmatic. Its anatomy is quite remarkable in that it receives input from almost all regions of cortex and projects back to almost all regions of cortex. We here briefly summarize what is known about the claustrum, speculate on its possible relationship to the processes that give rise to integrated conscious percepts, propose mechanisms that enable information to travel widely within the claustrum and discuss experiments to address these questions.     

Peduncle of Hydra and the heart of higher organisms share a common ancestral origin

The heart is assumed to have evolved as the organ for pumping blood. Here we report a pumping phenomenon in Hydra, a member of the phylum Cnidaria. We find that the peduncle, lower quarter of the body column, stores most of the gastrovascular fluid when the animal is an elongate form. Upon contraction of the polyp, the peduncle contracts and transfers the fluid into the rest of the cavity. We also find that Hydra RFamide III, a homolog of cardioexcitatory RFamide neuropeptides in higher organisms, elevates this transfer activity. Further, CnNk-2, a homolog of a cardiomuscular tissue marker Nkx-2.5, is expressed in the endodermal tissue of the peduncle. These observations indicate that the transfer of fluid by the peduncle has a similar neurological and genetic basis to the pumping of blood by the heart, suggesting that the Hydra peduncle and the heart of higher organisms share a common ancestral origin.