Jellyfish (medusae) are a distinctive life-cycle stage of medusozoan cnidarians. They are major marine predators, with integrated neurosensory, muscular and organ systems. The genetic foundations of this complex form are largely unknown. We report the draft genome of the hydrozoan jellyfish Clytia hemisphaerica and use multiple transcriptomes to determine gene use across life-cycle stages. Medusa, planula larva and polyp are each characterized by distinct transcriptome signatures reflecting abrupt life-cycle transitions and all deploy a mixture of phylogenetically old and new genes. Medusa-specific transcription factors, including many with bilaterian orthologues, associate with diverse neurosensory structures. Compared to Clytia, the polyp-only hydrozoan Hydra has lost many of the medusa-expressed transcription factors, despite similar overall rates of gene content evolution and sequence evolution. Absence of expression and gene loss among Clytia orthologues of genes patterning the anthozoan aboral pole, secondary axis and endomesoderm support simplification of planulae and polyps in Hydrozoa, including loss of bilateral symmetry. Consequently, although the polyp and planula are generally considered the ancestral cnidarian forms, in Clytia the medusa maximally deploys the ancestral cnidarian-bilaterian transcription factor gene complement.

Jellyfish (medusae) are a distinctive life-cycle stage of medusozoan cnidarians. They are major marine predators, with integrated neurosensory, muscular and organ systems. The genetic foundations of this complex form are largely unknown. We report the draft genome of the hydrozoan jellyfish Clytia hemisphaerica and use multiple transcriptomes to determine gene use across life-cycle stages. Medusa, planula larva and polyp are each characterised by distinct transcriptome signatures reflecting abrupt life cycle transitions, and all deploy a mixture of phylogenetically old and new genes. Medusa specific transcription factors, including many with bilaterian orthologs, associate with diverse neurosensory structures. Compared to Clytia, the polyp-only hydrozoan Hydra has lost many of the medusa-expressed transcription factors, despite similar overall rates of gene content and sequence evolution. Absence of expression and gene loss among Clytia orthologs of genes patterning the anthozoan aboral pole, secondary axis and endomesoderm support simplification of planulae and polyps in Hydrozoa, including loss of bilateral symmetry. Consequently, although the polyp and planula are generally ! 1 Gene order disruption in the hydrozoan lineageWe tested conservation of gene order between Clytia, Hydra, Nematostella and Branchiostoma floridae, a bilaterian showing a particularly slow rate of loss of syntenic blocks [25], by identifying conserved adjacent pairs of orthologs (see methods) shared between two genomes. Clytia shares most genes in adjacent pairs with Hydra (340), including myc2 and its target CAD [26]. Fewer pairs were conserved between Clytia and either Nematostella (36) or Branchiostoma (16). Although Nematostella, Hydra and Clytia, as cnidarians, are equally distant phylogenetically from Branchiostoma, the number of genes in adjacent pairs in Clytia/Branchiostoma (16) or Hydra/ Branchiostoma (13) is considerably smaller than in Nematostella/Branchiostoma (110). Similar trends emerged from analyses limited to orthologs identified in all four species (Ch/Hv 51; Ch/Nv 8; Ch/Bf 4; Nv/Bf 20), so our conclusions are not biased by an inability to detect more divergent orthologs. These numbers are all significant compared to the same analyses performed with a randomized Clytia gene order. Such conservation of adjacent gene pairs possibly relates to coordinated transcription, or enhancers being embedded in adjacent genes [27]. In contrast, none ! 3 ! 20 ! Supplementary figure 2: Hoechst staining (blue) of DNA in Clytia oocytes dissected from isolated gonads kept overnight in the dark and fixed, 35 minutes after exposing to light, for antitubulin immunofluorescence in red. The oocytes in a) and b), fixed using formaldehyde, are in the resting, meiotic prophase I arrested state, and t he duplicated chromosome pairs are clearly distinct in the dark oocyte nucleus (GV, Germinal Vesicle). The oocyte in c), fixed in cold methanol, has begun the maturation process, and the chromosomes are gathering on a microtubule aster. In each of ...