Cnidarians are astonishingly diverse in body form and lifestyle, including the presence of a jellyfish stage in medusozoans and its absence in anthozoans. Here, we sequence the genomes of Aurelia aurita (a scyphozoan) and Morbakka virulenta (a cubozoan) to understand the molecular mechanisms responsible for the origin of the jellyfish body plan. We show that the magnitude of genetic differences between the two jellyfish types is equivalent, on average, to the level of genetic differences between humans and sea urchins in the bilaterian lineage. About one-third of Aurelia genes with jellyfish-specific expression have no matches in the genomes of the coral and sea anemone, indicating that the polyp-to-jellyfish transition requires a combination of conserved and novel, medusozoa-specific genes. While no genomic region is specifically associated with the ability to produce a jellyfish stage, the arrangement of genes involved in the development of a nematocyte—a phylum-specific cell type—is highly structured and conserved in cnidarian genomes; thus, it represents a phylotypic gene cluster.

Abstract:The giant cubozoan Morbakka virulenta was collected from the central part of the Seto Inland Sea, western Japan in October 2009, in order to observe its development and polyp formation. Fertilization occurred externally. Demersal fertilized eggs were obtained during the incubation of mature females and males kept at a temperature of ca. 17 to 21°C. From the two-cell stage onwards, fertilized eggs developed into blastulae within 4 h. The development of the blastulae stopped for 21 days after forming blastocysts. This formation of blastocysts is up to now unique within the Cnidaria. The planulae, which developed inside the cysts and lacked larval ocelli, this being characteristic for the Cubozoa, finally metamorphosed into polyps bearing only a single tentacle. The 16-tentacledstage in polyps was reached about three months after this metamorphosis. Budding occurred in eight-tentacled polyps and swimming polyps were released nine days after the commencement of budding. These unique developmental features of M. virulenta may shed additional light on the evolution of life history strategies in the Cnidaria.

While records of Carybdea marsupialis in the literature suggest a worldwide distribution of this species, the validity of some of these records has been questioned recently, as has the validity of some nominal Carybdea species. We inspected material of all known species of Carybdea from multiple locations (i.e. Spain, Algeria, Tunisia, Puerto Rico, California, Hawaii, Australia, South Africa, and Japan) using morphological and genetic tools to differentiate Carybdea species as well as understand their evolutionary relationships. We observed morphological differences between adult medusae of Mediterranean and Caribbean C. marsupialis; the most obvious differences were the structure of the phacellae, the structure of the pedalial canal knee bend, and the number and structure of the velarial canals. The characters of the adult Mediterranean specimens agree with the description provided by Claus (1878) for individuals of C. marsupialis from the Adriatic Sea (Italy); specimens from the Caribbean (Puerto Rico) agreed with the description of C. xaymacana by Conant (1897). Significant differences between both species were also observed in the newly released medusa stage. Further, we resolved a discord about the undefined polyp culture originating from Puerto Rico that was long considered Carybdea marsupialis but should be referred to as C. xaymacana. Although C. marsupialis is currently considered the only species of Cubozoa to occur in the Mediterranean, specimens collected in Algeria and Tunisia suggest that species of Alatinidae may also be present in the Mediterranean. Our investigations indicate that Carybdea spp. are more restricted in their geographical distribution than has been recognized historically. These findings confirm that Carybdea arborifera Maas, 1897 from Hawaii, Carybdea branchi, Gershwin & Gibbons, 2009 from South Africa, Carybdea brevipedalia Kishinouye, 1891 from Japan, Carybdea confusa Straehler-Pohl, Matsumoto & Acevedo, 2017 from California, Carybdea marsupialis Linnaeus, 1758 from the European Mediterranean Sea, Carybdea rastonii Haacke, 1886 from South Australia, and Carybdea xaymacana, Conant, 1897 from the Caribbean Sea are valid names representing distinct species, rather than synonyms. A taxonomic key for all valid species is provided, and a neotype for C. marsupialis is designated.

The small box jellyfish Copula sivickisi was collected from the Ryukyu Archipelago, southern Japan, in June 2011, in order to observe its early life history, including polyp formation and metamorphosis. Fertilization occurred internally. Fertilized eggs were packed in an embryo strand with nematocysts and released into the water from the female s manubrium. Blastulae developed into planulae bearing about 30 larval ocelli within two days, and then settled and metamorphosed into primary polyps. Primary polyps developed into adult polyps within 40 days, and both polyp stages could actively detach to change location by creeping on the central part of their body. Adult polyps formed cysts at temperatures below 20°C, which when favorable conditions retuned (above 28°C), excysted from the capsules within a week. Budding occurred in adult polyps, and buds were released two days after the commencement of budding. Metamorphosis of a whole polyp into a single medusa occurred within 10 days. Juvenile medusae were distinguished from those of other cubozoans by the pattern of nematocyst warts on the exumbrella and the adhesive pads on the apex. The developmental features of C. sivickisi resemble most closely those of T. cystophora among the cubozoans. The similarities in all early life stages of both species support recent molecular results.

Both sexes of the Japanese giant box jellyfish Morbakka virulenta were collected from the Seto Inland Sea, western Japan in December 2011, in order to observe the developmental processes from polyps to medusae. The medusa production in M. virulenta is up to now a unique process in cubozoans in that it exhibits a form of monodisc strobilation where the polyp is regenerated before the medusa detaches. This mode of medusa production was previously thought to be exclusive to scyphozoans. The general shape of young medusae resembles that of other cubozoans such as Alatina moseri and Copula sivickisi, but is differentiated from these by the short capitate tentacles and the lack of gastric filaments in the stomach. The unique medusa production of M. virulenta highly implies a phylogenetic similarity between cubozoans and scyphozoans.