BackgroundThe phylogeny of Cnidaria has been a source of debate for decades, during which nearly all-possible relationships among the major lineages have been proposed. The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells, symbiosis, colonial body plans and elaborate life histories. However, understanding the origins and subsequent diversification of these traits remains difficult due to persistent uncertainty surrounding the evolutionary relationships within Cnidaria. While recent phylogenomic studies have advanced our knowledge of the cnidarian tree of life, no analysis to date has included genome-scale data for each major cnidarian lineage.ResultsHere we describe a well-supported hypothesis for cnidarian phylogeny based on phylogenomic analyses of new and existing genome-scale data that includes representatives of all cnidarian classes. Our results are robust to alternative modes of phylogenetic estimation and phylogenomic dataset construction. We show that two popular phylogenomic matrix construction pipelines yield profoundly different datasets, both in the identities and in the functional classes of the loci they include, but resolve the same topology. We then leverage our phylogenetic resolution of Cnidaria to understand the character histories of several critical organismal traits. Ancestral state reconstruction analyses based on our phylogeny establish several notable organismal transitions in the evolutionary history of Cnidaria and depict the ancestral cnidarian as a solitary, non-symbiotic polyp that lacked a medusa stage. In addition, Bayes factor tests strongly suggest that symbiosis has evolved multiple times independently across the cnidarian radiation.ConclusionsCnidaria have experienced more than 600 million years of independent evolution and in the process generated an array of organismal innovations. Our results add significant clarification on the cnidarian tree of life and the histories of some of these innovations. Further, we confirm the existence of Acraspeda (staurozoans plus scyphozoans and cubozoans), thus reviving an evolutionary hypothesis put forward more than a century ago.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1142-0) contains supplementary material, which is available to authorized users.

In nearly all animals, mitochondrial DNA (mtDNA) consists of a single circular molecule that encodes several subunits of the protein complexes involved in oxidative phosphorylation as well as part of the machinery for their expression. By contrast, mtDNA in species belonging to Medusozoa (one of the two major lineages in the phylum Cnidaria) comprises one to several linear molecules. Many questions remain on the ubiquity of linear mtDNA in medusozoans and the mechanisms responsible for its evolution, replication, and transcription. To address some of these questions, we determined the sequences of nearly complete linear mtDNA from 24 species representing all four medusozoan classes: Cubozoa, Hydrozoa, Scyphozoa, and Staurozoa. All newly determined medusozoan mitochondrial genomes harbor the 17 genes typical for cnidarians and map as linear molecules with a high degree of gene order conservation relative to the anthozoans. In addition, two open reading frames (ORFs), polB and ORF314, are identified in cubozoan, schyphozoan, staurozoan, and trachyline hydrozoan mtDNA. polB belongs to the B-type DNA polymerase gene family, while the product of ORF314 may act as a terminal protein that binds telomeres. We posit that these two ORFs are remnants of a linear plasmid that invaded the mitochondrial genomes of the last common ancestor of Medusozoa and are responsible for its linearity. Hydroidolinan hydrozoans have lost the two ORFs and instead have duplicated cox1 at each end of their mitochondrial chromosome(s). Fragmentation of mtDNA occurred independently in Cubozoa and Hydridae (Hydrozoa, Hydroidolina). Our broad sampling allows us to reconstruct the evolutionary history of linear mtDNA in medusozoans.

Cubozoa (Cnidaria: Medusozoa) represents a small clade of approximately 50 described species, some of which cause serious human envenomations. Our understanding of the evolutionary history of Cubozoa has been limited by the lack of a sound phylogenetic hypothesis for the group. Here, we present a comprehensive cubozoan phylogeny based on ribosomal genes coding for near-complete nuclear 18S (small subunit) and 28S (large subunit) and partial mitochondrial 16S. We discuss the implications of this phylogeny for our understanding of cubozoan venom evolution, biogeography and life-history evolution. Our phylogenetic hypothesis suggests that: (i) the last common ancestor of Carybdeida probably possessed the mechanism(s) underlying Irukandji syndrome, (ii) deep divergences between Atlantic and Indo-Pacific clades may be explained by ancient vicariant events, and (iii) sexual dimorphism evolved a single time in concert with complex sexual behaviour. Furthermore, several cubozoan taxa are either para-or polyphyletic, and we address some of these taxonomic issues by designating a new family, Carukiidae, a new genus, Copula, and by redefining the families Tamoyidae and Tripedaliidae. Lastly, cubozoan species identities have long been misunderstood and the data presented here support many of the recent scientific descriptions of cubozoan species. However, the results of a phylogeographic analysis of Alatina moseri from Hawai'i and Alatina mordens from Australia indicate that these two nominal species represent a single species that has maintained metapopulation cohesion by natural or anthropogenic dispersal.