The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution

Introduction An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. The phylogenetic relationship of ctenophores (comb jellies) to other animals has been a source of long-standing debate. Until recently, it was thought that Porifera (sponges) was the earliest diverging animal lineage, but recent reports have instead suggested Ctenophora as the earliest diverging animal lineage. Because ctenophores share some of the same complex cell types with bilaterians (such as neural and mesodermal cells), the phylogenetic position of ctenophores affects how we think about the early evolution of these cell types. The phylogenetic position of the ctenophore Mnemiopsis leidyi and its implications regarding the origin of mesodermal cell types. (A) Adult M. leidyi. (B) Summary of the relationships of the five main branches of animals and the outgroup Choanoflagellata. (C) Inventory of myogenic specification genes in Mnemiopsis. Components present in the Mnemiopsis genome are in blue, and names are underlined. Absent components are in red. The lack of many of these factors in Mnemiopsis indicates that ctenophore mesodermal cell types are specified differently than in bilaterians, suggesting that they perhaps evolved independently in these two lineages. Methods We have sequenced, annotated, and analyzed the 150-megabase genome of the ctenophore Mnemiopsis leidyi. We have performed detailed phylogenetic analyses on these new data using both sequence matrices and information on gene content. We conducted extensive genomic inventories on signaling pathway components and genes known to be critical to neural and mesodermal cell types, among others. Results Our phylogenetic analyses suggest that ctenophores are the sister group to the rest of the extant animals. We find that the sets of neural components present in the genomes of Mnemiopsis and the sponge Amphimedon queenslandica are quite similar, suggesting that sponges have the necessary genetic machinery for a functioning nervous system but may have lost these cell types. We also find that, although Mnemiopsis has most of the genes coding for structural components of mesodermal cells, they lack many of the genes involved in bilaterian mesodermal specification and, therefore, may have independently evolved these cell types. Discussion These results present a newly supported view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells. This evolutionary framework, along with the comprehensive genomic resources made available through this study, will yield myriad discoveries about our most distant animal relatives, many of which will shed light not only on the biology of these extant organisms but also on the evolutionary history of all animal species, including our own. The Base of the Animal Tree? The identity of the most basal lineages of the animal kingdom evolutionary tree has long been contested. Ryan et al. (p. 10.1126/science.1242592; see the Perspective by Rokas) sequenced the genome of the ctenophore the warty comb jelly or sea walnut, Mnemiopsis leidyi, and conclude that ctenophores alone, not sponges or the clade consisting of both ctenophores and cnidarians, are the most basal extant animals. The results suggest a specific evolutionary process that likely occurred—including repeated gains and loss of mesoderm, expansion of genes associated with the cell cycle, growth signaling, apoptosis, and epithelial and neural cell types. Furthermore, previous hypotheses regarding the evolution of animals may require re-evaluation. Analysis of the genome of the sea walnut reveals insights into the early evolution of the animal kingdom. [Also see Perspective by Rokas] An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. Toward this goal, we have sequenced, assembled, and annotated the genome of the ctenophore Mnemiopsis leidyi. Our phylogenomic analyses of both amino acid positions and gene content suggest that ctenophores rather than sponges are the sister lineage to all other animals. Mnemiopsis lacks many of the genes found in bilaterian mesodermal cell types, suggesting that these cell types evolved independently. The set of neural genes in Mnemiopsis is similar to that of sponges, indicating that sponges may have lost a nervous system. These results present a newly supported view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells.