The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution

Abstract

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.

Figure 1. Mnemiopsis leidyi life history and anatomy

a, Adult M. leidyi (approximately 10 cm long). b, Close view of comb rows. c, Aboral view of cydippid stage. d. One-celled fertilized embryo. e–h, Early cleavage stages. i, Gastrula stage. j–m, Later development of M. leidyi embryo. Panels j–m show oral side down. Embryos are approximately 200 microns. See SOM S1 for a more detailed description of the ctenophore body plan. Panel ‘a’ courtesy of Bruno Vellutini.

Figure 2. Previously proposed relationships of the five deep clades of animals

The label at the bottom of each pane corresponds to the header of Table 1. (a) Coelenterata hypothesis. (b) Ctenophora as sister to Bilateria. (c) Porifera as sister group to the rest of Metazoa. (d) Ctenophora as sister group to the rest of Metazoa. (e) Placozoa as sister group to the rest of Metazoa. (f) Diploblastica hypothesis. We see no support in our any of our analyses for the hypotheses in panels a, e, and f, and very little support for panel b (see Table 1). Ct = Ctenophora, Po = Porifera, Tr = Placozoa, Cn = Cnidaria, and Bi = Bilateria.

Figure 3. Tree produced by maximum-likelihood analysis of the EST Set

Tree was produced from a matrix consisting of 242 genes and 104,840 amino acid characters. Circles on nodes indicate 100% bootstrap support. Support placing ctenophores as sister to the rest of Metazoa is 96% of 100 bootstrap replicates.

Figure 4. Tree produced by maximum-likelihood analysis of gene content

Tree was produced from a matrix consisting of 23,910 binary characters indicating the presence or absence of a particular species within a cluster of genes. Clusters were produced with default settings of OrthoMCL. Columns consistent with known relationships within Bilateria were up-weighted while characters conflicting characters were down-weighted. Matrix was analyzed with RAxML under the GTR gamma model of rate heterogeneity. All nodes receive 100% bootstrap support. Constraining known relationships did not affect the position of Ctenophora (Fig. S4).

Figure 5. The origin of post-synaptic genes

A possible configuration for post-synaptic genes. Genes are colored by their node of origin (figure inset). Accession numbers of M. leidyi genes are in Table S16.

Figure 6. Inventory of myogenic components in Mnemiopsis leidyi

Components present in the M. leidyi genome are in blue and names are underlined. Absent components are in red. (A) The main structural components of smooth muscle are present in the M. leidyi genome. All structural components are present except for Troponin (in red). (B) The majority of signaling molecules and transcription factors involved in specifying and differentiating the mesoderm of bilaterian animals are absent from the genome of M. leidyi. The asterisks next to Snail and GATA indicate that these components have been identified in the transcriptomes of other ctenophores.