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.     

Dead-end evolution of the Cnidaria as deduced from 5S ribosomal RNA sequences

Using nucleotide sequences of 5S ribosomal RNAs from 2 hydrozoan jellyfishes, 3 scyphozoan jellyfishes and 2 sea anemones, a phylogenetic tree of Cnidaria has been constructed to elucidate the evolutionary relationships of radial and bilateral symmetries. The 3 classes of Cnidaria examined herein belong to one branch, which does not include other metazoan phyla such as the Platyhelminthes. The Hydrozoa (having radial symmetry without septa) and the Scyphozoa (having radial symmetry with septa) are more closely related to each other than to the Anthozoa (having bilateral symmetry with septa). In classical taxonomy, multicellular animals are considered to have evolved through organisms with radial symmetry (e.g., Cnidaria) to bilateral symmetry. Our results, however, indicate that the emergence of the Bilateria was earlier than that of the Radiata, suggesting (in opposition to Haeckel's view) that the radial symmetry of Cnidaria is an evolutionary dead end.     

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.     

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.].     

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.     

Placozoa are not derived cnidarians: evidence from molecular morphology

The phylum Placozoa is represented by a single known species, Trichoplax adhaerens, a tiny marine organism that represents the most simple metazoan bauplan. Because of the latter, placozoans were originally considered the most basal metazoan phylum. A misinterpretation of the life cycle at the turn of the century and some more recent molecular phylogenetic analyses have placed Trichoplax as a derived species within the Cnidaria. The latter hypothesis assumes that the primitive organization of the Placozoa is the result of secondary reduction. Here we compare the molecular morphology of the predicted 16S rDNA structure and the mitochondrial genome between Trichoplax and representatives of all four cnidarian classes. Trichoplax shares a circular mtDNA molecule as a plesiomorphy with all other metazoans except for the derived cnidarian classes Hydrozoa, Scyphozoa, and Cubozoa. The predicted secondary structure of the 16S rRNA molecule differs substantially between Trichoplax and cnidarians, particularly with respect to the number and length of stem and loop regions. The new molecular morphological characters provide compelling evidence that Trichoplax is not a derived (medusozoan) cnidarian. Furthermore, it was found that the mitochondrial genome in Cubozoa consists of four linear molecules instead of a single circular molecule or two linear molecules, suggesting that the cubozoans may represent the most derived cnidarian group.     

Evolutionary relationships among scyphozoan jellyfish families based on complete taxon sampling and phylogenetic analyses of 18S and 28S ribosomal DNA

A stable phylogenetic hypothesis for families within jellyfish class Scyphozoa has been elusive. Reasons for the lack of resolution of scyphozoan familial relationships include a dearth of morphological characters that reliably distinguish taxa and incomplete taxonomic sampling in molecular studies. Here, we address the latter issue by using maximum likelihood and Bayesian methods to reconstruct the phylogenetic relationships among all 19 currently valid scyphozoan families, using sequence data from two nuclear genes: 18S and 28S rDNA. Consistent with prior morphological hypotheses, we find strong evidence for monophyly of subclass Discomedusae, order Coronatae, rhizostome suborder Kolpophorae and superfamilies Actinomyariae, Kampylomyariae, Krikomyariae, and Scapulatae. Eleven of the 19 currently recognized scyphozoan families are robustly monophyletic, and we suggest recognition of two new families pending further analyses. In contrast to long-standing morphological hypotheses, the phylogeny shows coronate family Nausithoidae, semaeostome family Cyaneidae, and rhizostome suborder Daktyliophorae to be nonmonophyletic. Our analyses neither strongly support nor strongly refute monophyly of order Rhizostomeae, superfamily Inscapulatae, and families Ulmaridae, Catostylidae, Lychnorhizidae, and Rhizostomatidae. These taxa, as well as familial relationships within Coronatae and within rhizostome superfamily Inscapulatae, remain unclear and may be resolved by additional genomic and taxonomic sampling. In addition to clarifying some historically difficult taxonomic questions and highlighting nodes in particular need of further attention, the molecular phylogeny presented here will facilitate more robust study of phenotypic evolution in the Scyphozoa, including the evolution characters associated with mass occurrences of jellyfish.     

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.     

Phospholipase A2 in cnidaria

Phospholipase A2 (PLA2) is an enzyme present in snake and other venoms and body fluids. We measured PLA2 catalytic activity in tissue homogenates of 22 species representing the classes Anthozoa, Hydrozoa, Scyphozoa and Cubozoa of the phylum Cnidaria. High PLA2 levels were found in the hydrozoan fire coral Millepora sp. (median 735 U/g protein) and the stony coral Pocillopora damicornis (693 U/g) that cause skin irritation upon contact. High levels of PLA2 activity were also found in the acontia of the sea anemone Adamsia carciniopados (293 U/g). Acontia are long threads containing nematocysts and are used in defense and aggression by the animal. Tentacles of scyphozoan and cubozoan species had high PLA2 activity levels: those of the multitentacled box jellyfish Chironex fleckeri contained 184 U/g PLA2 activity. The functions of cnidarian PLA2 may include roles in the capture and digestion of prey and defense of the animal. The current observations support the idea that cnidarian PLA2 may participate in the sting site irritation and systemic envenomation syndrome resulting from contact with cnidarians.     

Phylogenetics and evolution of Capitata (Cnidaria: Hydrozoa), and the systematics of Corynidae

Nawrocki, A. M., Schuchert, P. & Cartwright, P. (2009). Phylogenetics and evolution of Capitata (Cnidaria: Hydrozoa), and the systematics of Corynidae.—Zoologica Scripta, 39, 290–304. Generic‐ and family level classifications in Hydrozoa have been historically problematic due to limited morphological characters for phylogenetic analyses and thus taxonomy, as well as disagreement over the relative importance of polyp vs. medusa characters. Within the recently redefined suborder Capitata (Cnidaria: Hydrozoa: Hydroidolina), which includes 15 families and almost 200 valid species, family level relationships based on morphology alone have proven elusive, and there exist numerous conflicting proposals for the relationships of component species. Relationships within the speciose capitate family Corynidae also remain uncertain, for similar reasons. Here, we combine mitochondrial 16S, and nuclear 18S and 28S sequences from capitate hydrozoans representing 12 of the 15 valid capitate families, to examine family level relationships within Capitata. We further sample densely within Corynidae to investigate the validity of several generic‐level classification schemes that rely heavily on the presence/absence of a medusa, a character that has been questioned for its utility in generic‐level classification. We recover largely congruent tree topologies from all three markers, with 28S and the combined dataset providing the most resolution. Our study confirms the monophyly of the redefined Capitata, and provides resolution for family level relationships of most sampled families within the suborder. These analyses reveal Corynidae as paraphyletic and suggest that the limits of the family have been underestimated. Our results contradict all available generic‐level classification schemes for Corynidae. As classification schemes for this family have been largely based on reproductive characters such as the presence/absence of a medusa, our results suggest that these are not valid generic‐level characters for the clade. We suggest a new taxonomic structure for the lineage that includes all members of the newly redefined Corynidae, based on molecular and morphological synapomorphies for recovered clades within the group.     

Phylogeny of the Plumularioidea (Hydrozoa, Leptothecata): evolution of colonial organisation and life cycle

The Plumularioidea (Cnidaria, Hydrozoa, Leptothecata) are the most species rich superfamily of the class Hydrozoa. They display a complex and diversified colonial organisation and their life cycle comprises either a reduced free-living, pelagic generation (medusoid), alternating with the benthic colonial form or in most species, no pelagic generation. In order to understand the evolution of colonial and life cycle characters among Plumularioidea, we have reconstructed their phylogeny. Partial mitochondrial 16S rRNA sequences and 64 morphological characters were analysed separately and in combination. The morphological data included not only characters of the individual polyps and medusae, but also characters describing the organisation of colonies, for which we propose general principles applying to character coding in modular organisms. The phylogenetic analyses supported the monophyly of Plumularioidea and of the four plumularioid families (Aglaopheniidae, Halopterididae, Kirchenpaueriidae and Plumulariidae). Most genera were paraphyletic or polyphyletic. This study highlights multiple morphological simplifications of the colonial organisation during the evolution of Plumularioidea and the convergence of the defensive polyps — the dactylozooids — of Plumularioidea with those of others Leptothecata ( Hydrodendron ) or Anthoathecata ( Hydractinia ). Concerning the evolution of the life cycle, the phylogeny supports a provocative scenario, where the medusa was lost in an ancestor of the Plumularioidea, and then re-acquired four times independently within this group, in the form of simple medusoids.     

Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees

To elucidate the evolution of one of the most species-rich ant-plant symbiotic systems, the association between Crematogaster (Myrmicinae) and Macaranga (Euphorbiaceae) in South-East Asia, we conducted a phylogenetic analysis of the ant partners. For the phylogenetic analysis partial mitochondrial cytochrome oxidase I and II were sequenced and Maximum Parsimony analysis was performed. The analyzed Crematogaster of the subgenus Decacrema fell into three distinct clades which are also characterized by specific morphological and ecological traits (queen morphology, host-plants, and colony structure). Our results supported the validity of our currently used morphospecies concept for Peninsula Malaysia. However, on a wider geographic range (including North and North-East Borneo) some morphospecies turned out to be species complexes with genetically quite distinct taxa. Our phylogenetic analysis and host association studies do not indicate strict cocladogenesis between the subgenus Decacrema and their Macaranga host-plants because multiple ant taxa occur on quite distinct host-plants belonging to different clades within in the genus Macaranga. These results support the view that host-shifting or host-expansion is common in the ants colonizing Macaranga. Additionally, the considerable geographic substructuring found in the phylogenetic trees of the ants suggests that allopatric speciation has also played a role in the diversification and the current distribution of the Decacrema ants.     

Internal phylogeny of the Chilopoda (Myriapoda, Arthropoda) using complete 18S rDNA and partial 28S rDNA sequences

The internal phylogeny of the 'myriapod' class Chilopoda is evaluated for 12 species belonging to the five extant centipede orders, using 18S rDNA complete gene sequence and 28S rDNA partial gene sequence data. Equally and differentially weighted parsimony, neighbour-joining and maximum-likelihood were used for phylogenetic reconstruction, and bootstrapping and branch support analyses were performed to evaluate tree topology stability. The results show that the Chilopoda constitute a monophyletic group that is divided into two lines, Notostigmophora (= Scutigeromorpha) and Pleurostigmophora, as found in previous morphological analyses. The Notostigmophora are markedly modified for their epigenic mode of life. The first offshoot of the Pleurostigmophora are the Lithobiomorpha, followed by the Craterostigmomorpha and by the Epimorpha s. str. (= Scolopendromorpha + Geophilomorpha), although strong support for the monophyly of the Epimorpha s. lat. (= Craterostigmomorpha + Epimorpha s. str.) is only found in the differentially weighted parsimony analysis.     

Simultaneous analysis of the basal lineages of Hymenoptera (Insecta) using sensitivity analysis

The first simultaneous analysis of molecular and morphological data of basal hymenopterans that includes exemplars from all families is presented. DNA sequences (of approximately 2000–2700 bp for each taxon) from the nuclear genes 18S and 28S and the mitochondrial genes 16S and CO1 have been sequenced for 39 taxa (four outgroup taxa, 29 symphytans, and six apocritans). These DNA sequences and 236 morphological characters from Vihelmsen [Zool. J. Linnean Soc. 131 (2001) 393] were analyzed separately as well as simultaneously. All analyses were performed on unaligned sequences, using the optimization alignment (= direct optimization) method. Sensitivity analysis sensu Wheeler [Syst. Biol. 44 (1995) 321] was applied by analyzing the data under nine different combinations of analysis parameter values. The superfamily level relationships of basal hymenopterans as proposed by Vilhelmsen [Zool. J. Linnean Soc. 131 (2001) 393] and Ronquist et al. [Zool. Scr. 28 (1999) 13] are mostly confirmed, except that Pamphilioidea is the sister group to Tenthredinoidea s.l. and that Anaxyelidae (i.e., Syntexis libocedrii) and Siricidae are supported as a monophyletic group, partly reestablishing the traditional concept of Siricoidea. The resulting hypothesis that best represents the combined evidence from morphology and DNA sequences is (Xyeloidea (Tenthredinoidea s.l. Pamphilioidea) (Cephoidea (Siricoidea (Xiphydrioidea (Orussidae Apocrita))))), with Siricoidea = Anaxyelidae +Siricidae. The phylogenetic system within Tenthredinoidea s.l., derived from the combined evidence, is (Blasticotomidae (Tenthredinidae including Diprionidae (Cimbicidae (Argidae Pergidae)))).     

Myzostomida Are Not Annelids: Molecular and Morphological Support for a Clade of Animals with Anterior Sperm Flagella

The myzostomes are animals with five pairs of parapodia, living as commensals or (endo)parasites mostly on crinoid and ophiuroid echinoderms. They are generally considered aberrant annelids, possibly phyllodocidan polychaetes. A phylogenetic analysis of 18S and 28S ribosomal DNA sequence data of Myzostoma glabrum , together with 60 morphological, developmental, ultrastructural, and life-history characters, is presented to show that myzostomes are a sister group of the Cycliophora, closely related to the rotifer-acanthocephalan clade (=Syndermata). Myzostomes and syndermates share predominantly the highly derived spermatozoa with anteriorly directed flagella (cycliophoran sperm is insufficiently known). The myzostome-cycliophoran-syndermate clade, accommodated within the Platyzoa (including Platyhelminthes s. str. , Gastrotricha, Gnathostomulida, Syndermata, Cycliophora, and Myzostomida), is strongly supported by most analyses, regardless of alignment parameters, character combinations and weighting, species sampling, and tree-building methods. The new name Prosomastigozoa ("forward-flagellar animals") is proposed for the group including three phyla (Cycliophora, Myzostomida, and Syndermata).     

New data on the morphology of Sphenothallus Hall: implications for its affinities

Van Iten, H., Cox, R. S. & Mapes, R. H. 1992 04 15: New data on the morphology of Sphenothallus Hall: implications for its affinities. Lethaia , Vol. 25, pp. 135–144. Oslo. ISSN 0024–1164.
Recent speculation on the phylogenetic relationships of Sphenothallus Hall, 1847 has focused on two alternatives: (1) affinity with hydrozoan or scyphozoan cnidarians, or (2) affinity with annelids or other 'worms'. We have found that some species of Sphenothallus formed branching clonal colonies, and that others produced a thin transverse wall, similar to the conulariid schott. Sphenothallus tests are composed of carbonate apatite and are built of numerous, extremely thin lamellae (< 1 μm) that parallel the surface of the test. The holdfast, long interpreted as consisting of a pair of nested cups, actually consists of a single closed, broadly conical expansion floored by a thin basal membrane. Many thecate hydrozoan and scyphozoan polyps form branching clonal colonies and produce a thin transverse wall, similar to that produced by Sphenothallus . Further, thecae of coronatid scyphozoans are built of submicron-thick lamellae that parallel the outer surface of the theca, and coronatid thecae possess a closed, broadly conical apical expansion that serves as a holdfast. No such combination of characteristics exists among annelids or other non-cnidarian taxa. The recent discovery of paired tentacles in Sphenofhallus from the Early Devonian Hunsrück Slate by Fauchald et al ., thought to indicate that Sphenorhallus was wormlike, does not militate against a hypothesis of affinity with cnidarians. We therefore favour the hypothesis of a cnidarian affinity for Sphenothallus. * Sphenothallus, vermiform problematica, phylogenetic inference, coloniality, Cnidoria, Hydrozoa, Scyphozoa, Annelida, conulariids, byroniids, Bear Gulch Limestone .     

Morphology and systematics in mesopsammic nemerteans of the genus Ototyphlonemertes (Nemertea,Hoplonemertea, Ototyphlonemertidae)

Interstitial nemerteans of the genus Ototyphlonemertes are difficult to organize into traditional morphospecies. They occur in a multitude of slightly different local varieties that form a seemingly continuous morphological cline. In this paper, we summarize most published morphological data on the group, plus 73 new records of geographic varieties from the Mediterranean Sea in the East to the Sea of Japan in the West. We summarize morphological variation, partition traits into character and character states, propose a standardized protocol for examination of live specimens and discuss the phylogenetic structure of the group. The phylogenetic discussion leads to a hypothesis that partitions all varieties (including the established species) into six groups. These are the smallest morphologically homogenous sets of varieties (corresponding to traditional morphospecies) we can diagnose on phylogenetically reliable traits. Variation within the groups appears to be unreliable phylogenetic markers that may distinguish ecological forms rather than relatedness. However, we distinguish four of the groups by combinations of two traits, one apomorphy for a more inclusive group and one plesiomorphy, and the remaining two by one trait each that may be either a unique plesiomorphy or an apomorphy depending on the rooting, and most of them may thus join paraphyletic groups of cryptic monophyletic units. We call this kind of group phylomorph and name them the Duplex-, Pallida-, Cirrula-, Fila-, Lactea- and Macintoshi-morph (referring to the first established species within each group, i.e. Ototyphlonemertes duplex, O. pallida, O. cirrula, O. fila, O. lactea and O. macintoshi respectively). The phylogenetic scheme provides a simple tool to allocate geographical varieties to a group of possible `species' and a phylogenetic null-hypothesis for further tests with genetic data.