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.     

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.     

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.     

Trachylina: The Group That Remains Enigmatic Despite 150 Years of Investigations

Trachylina is a group of cnidarians, a subclass of Hydrozoa. Despite the low species diversity of this group, its representatives are characterized by diversity of life cycles. Trachylina have populated various environments, from deep ocean to fresh water ecosystems. Polyps of Trachylina are either very small or absent in the life cycle, which distinguishes this group from the majority of other Hydrozoa. Trachylina are also highly diverse and have a number of features that are unusual for cnidarians. A number of representatives of this group are characterized by a small number of cells at the embryonic and larval stages. This phenomenon is well known for the representatives of phylogenetically distant taxa—Nematoda and Chordata (Tunicata). In addition, the development of Trachylina is characterized by a number of evolutionary changes that, apparently, make it possible to accelerate the formation of the definitive stage (medusa). Paradoxically, there is no one species among the representatives of this group that is studied in more or less detail. The purpose of our review is to summarize the scanty information on the Trachylina ontogeny and to demonstrate the importance of studying the ontogeny of this group for understanding the general rules of the evolution of development and life cycles of Metazoa.     

Phylogeny of Capitata and Corynidae (Cnidaria, Hydrozoa) in light of mitochondrial 16S rDNA data

New sequences of the partial rDNA gene coding for the mitochondrial large ribosomal subunit, 16S, are derived from 47 diverse hydrozoan species and used to investigate phylogenetic relationships among families of the group Capitata and among species of the capitate family Corynidae. Our analyses identify a well-supported clade, herein named Aplanulata, of capitate hydrozoans that are united by the synapomorphy of undergoing direct development without the ciliated planula stage that is typical of cnidarians. Aplanulata includes the important model organisms of the group Hydridae, as well as species of Candelabridae, Corymorphidae, and Tubulariidae. The hypothesis that Hydridae is closely related to brackish water species of Moerisiidae is strongly controverted by 16S rDNA data, as has been shown for nuclear 18S rDNA data. The consistent phylogenetic signal derived from 16S and 18S data suggest that both markers would be useful for broad-scale multimarker analyses of hydrozoan relationships. Corynidae is revealed as paraphyletic with respect to Polyorchidae, a group for which information about the hydroid stage is lacking. Bicorona , which has been classified both within and outside of Corynidae, is shown to have a close relationship with all but one sampled species of Coryne . The corynid genera Coryne , Dipurena , and Sarsia are not revealed as monophyletic, further calling into question the morphological criteria used to classify them. The attached gonophores of the corynid species Sarsia lovenii are confirmed as being derived from an ancestral state of liberated medusae. Our results indicate that the 16S rDNA marker could be useful for a DNA-based identification system for Cnidaria, for which it has been shown that the commonly used cytochrome c oxidase subunit 1 gene does not work.     

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.     

Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly

Of the three major bilaterian clades, Lophotrochozoa has the greatest diversity and disparity of body forms and is the least understood in terms of phylogenetic history. Within this clade, small nuclear ribosomal subunit (SSU or 18S) studies have failed to provide resolution and other molecular markers have insufficient taxon sampling. To examine relationships within Lophotrochozoa, we collected and complied complete SSU data and nearly complete (>90%) large nuclear ribosomal subunit (LSU or 28S) data totaling approximately 5kb per taxon, for 36 lophotrochozoans. Results of LSU and combined SSU+LSU likelihood analyses provide topologies more consistent with morphological data than analyses of SSU data alone. Namely, most phyla recognized on morphological grounds are recovered as monophyletic entities when the LSU data is considered (contra SSU data alone). These new data show with significant support that "Lophophorata" (traditionally recognized to include Brachiopoda, Phoronida, and Bryozoa) is not a monophyletic entity. Further, the data suggest that Platyzoa is real and may be derived within lophotrochozans rather than a basal or sister taxon. The recently discovered Cycliophora are allied to entoprocts, consistent with their initial placement based on morphology. Additional evidence for Syndermata (i.e., Rotifera+Acanthocephala) is also found. Although relationships among groups with trochophore-like larvae could not be resolved and nodal support values are generally low, the addition of LSU data is a considerable advance in our understanding of lophotrochozoan phylogeny from the molecular perspective.     

Phylogeny and morphological evolution of the so‐called bougainvilliids (Hydrozoa,Hydroidolina)

We present phylogenetic analyses (parsimony, maximum likelihood and Bayesian inference) for 69 lineages of anthoathecate hydroids based on 18 morphological characters (12 proposed for the first time) plus mitochondrial (16S and COI) and nuclear (18S and 28S) molecular markers. This study aims to test the monophyly of the present concept of the family Bougainvilliidae, assessing its phylogenetic position within Hydroidolina. Our working hypothesis is used as a context for inferring the evolution of certain morphological characters, focusing on the exoskeleton. Our results shed light on some phylogenetic uncertainties within Hydroidolina, delimiting eight well‐supported linages, viz. Hydroidolina, Siphonophorae, Leptothecata, Aplanulata, Filifera II, Filifera III, Capitata and Pseudothecata taxon novum, the latter supported by four morphological synapomorphies. The monophyly of several families was not supported, viz. Bougainvilliidae, Cordylophoridae, Oceaniidae, Rathkeidae and Pandeidae. Some of the genera typically considered in Bougainvilliidae, including Bougainvillia, fell into the clade Pseudothecata, which is consistently reconstructed as the sister group of Leptothecata. We formally suggest that Dicoryne be removed from Bougainvilliidae and placed in the resurrected family Dicorynidae. The exoskeleton was a key feature in the diversification of Hydroidolina, especially with the transition from the bare hydranth to one completely enveloped within the exoskeleton. In this context, bougainvilliids exhibit several intermediate states in the development of the exosarc. Although the concatenated analysis unravels some interesting hypotheses, taxon sampling is still deficient and therefore more data are necessary for achieving a more complete understanding of the evolution and ecology of bougainvilliids and their allies.     

Independent terrestrial origins of the Halosphaeriales (marine Ascomycota)

A phylogenetic study of marine ascomycetes was initiated to test and refine evolutionary hypotheses of marine-terrestrial transitions among ascomycetes. Taxon sampling focused on the Halosphaeriales, the largest order of marine ascomycetes. Approximately 1050 base pairs (bp) of the gene that codes for the nuclear small subunit (SSU) and 600 bp of the gene that codes for the nuclear large subunit (LSU) ribosomal RNAs (rDNA) were sequenced for 15 halosphaerialean taxa and integrated into a data set of homologous sequences from terrestrial ascomycetes. An initial set of phylogenetic analyses of the SSU rDNA from 38 taxa representing 15 major orders of the phylum Ascomycota confirmed a close phylogenetic relationship of the halosphaerialean species with several other orders of perithecial ascomycetes. A second set of analyses, which involved more intensive taxon sampling of perithecial ascomycetes, was performed using the SSU and LSU rDNA data in combined analyses. These second analyses included 15 halosphaerialean taxa, 26 terrestrial perithecial fungi from eight orders, and five outgroup taxa from the Pezizales. In these analyses the Halosphaeriales were polyphyletic and comprised two distinct lineages. One clade of Halosphaeriales comprised 12 taxa from 11 genera and was most closely related to terrestrial fungi of the Microascales. The second clade of halosphaerialean fungi comprised taxa from the genera Lulworthia and Lindra and was an isolated lineage among the perithecial fungi. Both the main clade of Halosphaeriales and the Lulworthia/Lindra clade are supported by the data as being independently derived from terrestrial ancestors.     

Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria)

The Campanulariidae is a group of leptomedusan hydroids (Hydrozoa, Cnidaria) that exhibit a diverse array of life cycles ranging from species with a free medusa stage to those with a reduced or absent medusa stage. Perhaps the best-known member of the taxon is Obelia which is often used as a textbook model of hydrozoan life history. However, Obelia medusae have several unique features leading to a hypothesis that Obelia arose, in a saltational fashion, from an ancestor that lacked a medusa, possibly representing an example of a rare evolutionary reversal. To address the evolution of adult sexual stages in Campanulariidae, a molecular phylogenetic approach was employed using two nuclear (18S rDNA and calmodulin) and two mitochondrial (16S rDNA and cytochrome c oxidase subunit I) genes. Prior to the main analysis, we conducted a preliminary analysis of leptomedusan taxa which suggests that Campanulariidae as presently considered needs to be redefined. Campanulariid analyses are consistent with morphological understanding in that three major clades are recovered. However, several recognized genera are not monophyletic calling into question some "diagnostic" features. Furthermore, ancestral states were reconstructed using parsimony, and a sensitivity analysis was conducted to investigate possible evolutionary transitions in life-history stages. The results indicate that life-cycle transitions have occurred multiple times, and that Obelia might be derived from an ancestor with Clytia-like features.     

Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae

To date, species identification of lichen photobionts has been performed principally on the basis of microscopic examinations and molecular data from nuclear-encoded genes. In plants, the chloroplast genome has been more readily exploited than the nuclear genome for systematic investigations. At the present time, very little information is available about the chloroplast genome of lichen-forming algae. For this reason, we have sequenced a portion of the gene encoding for the chloroplast large sub-unit rRNA (LSU rDNA) as a new molecular marker. Sequencing of the chloroplast LSU rDNAs revealed the existence of an unusual diversity of group I introns (a total of 31) within 15 analyzed Trebouxia species. The number, sequence and insertion site of these introns were very different among species, contributing to their recognition. A relatively large intron-free portion of the chloroplast LSU rDNA and part of the nuclear ribosomal cistron (18S–5.8S–26S) between the nuclear internal transcribed spacers (nrITS) were subjected to phylogenetic analyses. The obtained results indicate that data combination from both nuclear and chloroplast sequences can improve phylogenetic accuracy. Herein, we propose the suitability of both intronic and exonic sequences of the chloroplast LSU rDNA for species recognition, and an exonic sequence spanning from position 879 to 1837 in the Escherichia coli 23S rDNA for phylogenetic analyses of Trebouxia phycobionts.     

Informative characteristics of 12 divergent domains in complete large subunit rDNA sequences from the harmful dinoflagellate genus, Alexandrium (Dinophyceae)

The genus Alexandrium includes organisms of interest, both for the study of dinoflagellate evolution and for their impacts as toxic algae affecting human health and fisheries. Only partial large subunit (LSU) rDNA sequences of Alexandrium and other dinoflagellates are available, although they contain much genetic information. Here, we report complete LSU rDNA sequences from 11 strains of Alexandrium, including Alexandrium affine, Alexandrium catenella, Alexandrium fundyense, Alexandrium minutum, and Alexandrium tamarense, and discuss their segmented domains and structure. Putative LSU rRNA coding regions were recorded to be around 3,400 bp long. Their GC content (about 43.7%) is among the lowest when compared with other organisms. Furthermore, no AT-rich regions were found in Alexandrium LSU rDNA, although a low GC content was recorded within the LSU rDNA. No intron-like sequences were found. The secondary structure of the LSU rDNA and parsimony analyses showed that most variation in LSU rDNA is found in the divergent (D) domains with the D2 region being the most informative. This high D domain variability can allow members of the diverse Alexandrium genus to be categorized at the species level. In addition, phylogenetic analysis of the alveolate group using the complete LSU sequences strongly supported previous findings that the dinoflagellates and apicomplexans form a clade.     

Evolutionary relationships of the cup-fungus genus Peziza and Pezizaceae inferred from multiple nuclear genes: RPB2, beta-tubulin, and LSU rDNA

To provide a robust phylogeny of Pezizaceae, partial sequences from two nuclear protein-coding genes, RPB2 (encoding the second largest subunit of RNA polymerase II) and beta-tubulin, were obtained from 69 and 72 specimens, respectively, to analyze with nuclear ribosomal large subunit RNA gene sequences (LSU). The three-gene data set includes 32 species of Peziza, and 27 species from nine additional epigeous and six hypogeous (truffle) pezizaceous genera. Analyses of the combined LSU, RPB2, and beta-tubulin data set using parsimony, maximum likelihood, and Bayesian approaches identify 14 fine-scale lineages within Pezizaceae. Species of Peziza occur in eight of the lineages, spread among other genera of the family, confirming the non-monophyly of the genus. Although parsimony analyses of the three-gene data set produced a nearly completely resolved strict consensus tree, with increased confidence, relationships between the lineages are still resolved with mostly weak bootstrap support. Bayesian analyses of the three-gene data, however, show support for several more inclusive clades, mostly congruent with Bayesian analyses of RPB2. No strongly supported incongruence was found among phylogenies derived from the separate LSU, RPB2, and beta-tubulin data sets. The RPB2 region appeared to be the most informative single gene region based on resolution and clade support, and accounts for the greatest number of potentially parsimony informative characters within the combined data set, followed by the LSU and the beta-tubulin region. The results indicate that third codon positions in beta-tubulin are saturated, especially for sites that provide information about the deeper relationships. Nevertheless, almost all phylogenetic signal in beta-tubulin is due to third positions changes, with almost no signal in first and second codons, and contribute phylogenetic information at the "fine-scale" level within the Pezizaceae. The Pezizaceae is supported as monophyletic in analyses of the three-gene data set, but its sister-group relationships is not resolved with support. The results advocate the use of RPB2 as a marker for ascomycete phylogenetics at the inter-generic level, whereas the beta-tubulin gene appears less useful.     

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.     

Genetic Diversity and Evolution of Chinese Traditional Medicinal Fungus Polyporus umbellatus (Polyporales,Basidiomycota)

Background

Polyporus umbellatus is an important medicinal fungus distributed throughout most area of China. Its wide distribution may have resulted in substantial intraspecific genetic diversity for the fungus, potentially creating variation in its medical value. To date, we know little about the intraspecific genetic diversity of P. umbellatus.

Methodology/Principal Findings

The objective of this research was to assess genetic differences of P. umbellatus from geographically diverse regions of China based on nrDNA ITS and 28S rRNA (LSU, large subunit) sequences. Significant sequence variations in the ITS and LSU sequences were detected. All sclerotial samples were clustered into four clades based on phylogenetic analysis of ITS, LSU and a combined data set of both regions. Heterogeneity of ITS and LSU sequences was detected in 5 and 7 samples respectively. All clone sequences clustered into the same clade except for one LSU clone sequences (from Henan province) which clustered into two clades (Clade I and Clade II). Significant genetic divergence in P. umbellatus was observed and the genetic diversification was greater among sclerotial samples from Shaanxi, Henan and Gansu provinces than among other provinces. Polymorphism of ITS and LSU sequences indicated that in China, P. umbellatus may spread from a center (Shaanxi, Henan and Gansu province) to other regions.

Conclusions/Significance

We found sclerotial samples of P. umbellatus contained levels of intraspecific genetic diversity. These findings suggested that P. umbellatus populations in Shaanxi, Henan and Gansu are important resources of genetic diversity and should be conserved accordingly.     

Phylogenetic placement of <Emphasis Type="Italic">Marasmiellus juniperinus</Emphasis>

Recent collections and the type specimen of Marasmiellus juniperinus, the type species of the genus, were examined. Phylogenetic placement, based on ribosomal large subunit (LSU) and internally transcribed spacer (ITS) sequences, is within the lentinuloid clade, nested among Gymnopus taxa. This placement dictates genus name usage and phylogenetic position of other putative species of Marasmiellus. The mating system is tetrapolar.