Early animal evolution: Insights from genomes and embryos of cnidarians, placozoans and sponges

Since the origin of animals ∼750 million years ago, morphologically diverse animal forms have evolved. Sponges, cnidarians and placozoans are early diverging animal phyla and studies of their genomes and development can inform us on the transitions that generated the distinct body plans of these animals and of bilaterians (animals with bilateral symmetry). This manuscript describes analyses on the genomes of the Nematostella vectensis, the placozoan Trichoplax adhaerens, and the demosponge Amphimedon queenslandica in a comparative framework and presents experiments to test hypotheses generated by the genomic studies.;Whole-genome sequence data place placozoans as the sister-group to cnidarians and bilaterians, with sponges forming the earliest diverging animals. The genomes of Nematostella, Trichoplax and Amphimedon have retained a large proportion of the introns inferred for the eukaryotic ancestor. There is evidence of conserved synteny between the human genome and the genomes of Nematostella, Trichoplax, and Amphimedon. Thus, with regard to intron-exon gene structures and the organization of genes relative to each other, cnidarian, placozoan, and sponge genomes are more similar to our genome than the genomes of fruit flies and nematodes are.;Most major classes of developmental transcription factors and signaling genes are found in Nematostella, Trichoplax, and Amphimedon, suggesting that the common ancestor of all animals was likely endowed with a "toolkit" that possibly functioned in the execution of its developmental program. The origins of animal genes can be traced---most were ancient eukaryotic proteins, many were novel to the animal lineage, and many expanded over the course of early animal evolution.;Though their genomes harbor genes that pattern specific cell-types and structures in bilaterians, cnidarians, placozoans, and sponges lack morphologically recognizable counterparts of these cells/structures. For example, cnidarians have neurons that are not organized into a centralized nervous system, and placozoans and sponges don't have neurons yet their genomes have many genes for neural patterning and function. Neural markers reveal that Nematostella vectensis has functionally distinct neuronal populations that are regionalized along the oral-aboral axis. LIM homeobox (Lhx) transcription factors are a novel animal family that diversified before the radiation of animals and may pattern neuronal identity in Nematostella.