The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa

Abstract

BackgroundThe much-debated phylogenetic relationships of the five early branching metazoan lineages (Bilateria, Cnidaria, Ctenophora, Placozoa and Porifera) are of fundamental importance in piecing together events that occurred early in animal evolution. Comparisons of gene content between organismal lineages have been identified as a potentially useful methodology for phylogenetic reconstruction. However, these comparisons require complete genomes that, until now, did not exist for the ctenophore lineage. The homeobox superfamily of genes is particularly suited for these kinds of gene content comparisons, since it is large, diverse, and features a highly conserved domain.ResultsWe have used a next-generation sequencing approach to generate a high-quality rough draft of the genome of the ctenophore Mnemiopsis leidyi and subsequently identified a set of 76 homeobox-containing genes from this draft. We phylogenetically categorized this set into established gene families and classes and then compared this set to the homeodomain repertoire of species from the other four early branching metazoan lineages. We have identified several important classes and subclasses of homeodomains that appear to be absent from Mnemiopsis and from the poriferan Amphimedon queenslandica. We have also determined that, based on lineage-specific paralog retention and average branch lengths, it is unlikely that these missing classes and subclasses are due to extensive gene loss or unusually high rates of evolution in Mnemiopsis.ConclusionsThis paper provides a first glimpse of the first sequenced ctenophore genome. We have characterized the full complement of Mnemiopsis homeodomains from this species and have compared them to species from other early branching lineages. Our results suggest that Porifera and Ctenophora were the first two extant lineages to diverge from the rest of animals. Based on this analysis, we also propose a new name - ParaHoxozoa - for the remaining group that includes Placozoa, Cnidaria and Bilateria.

Convergent evolution of neural systems in ctenophores

“…Yes, these genes are present in ctenophore genomes but they cannot be considered as pan-neuronal markers in ctenophores because they are expressed in many other cell types. Plus their neuronal colocalization at the cellular level has not been shown (Jager et al, 2006;Derelle and Manuel, 2007;Jager et al, 2008;Ryan et al, 2010;Simmons et al, 2012;Schnitzler et al, 2014). The fact that some of these genes are associated with the aboral organ or polar fields does not mean that in these structures these genes are expressed in neurons (e.g.…”

The Holo-Transcriptome of a Calcified Early Branching Metazoan

“…The genome of the demosponge Amphimedon queenslandica contains several NK genes linked in a cluster but no Hox or ParaHox genes (Larroux et al, 2007). Due to the lack of Hox and ParaHox genes in both Amphimedon and the ctenophore Mnemiopsis leidyi the origin of Hox and ParaHox genes have been proposed to have occurred after the divergences of sponges and ctenophores from all other animals (Larroux et al, 2007;Ryan et al, 2010). On the other hand, the lack of Hox and ParaHox genes has been interpreted as gene loss as the genome of Amphimedon possesses distinct Hox and ParaHox neighborhoods (so called ghost loci) (Ramos et al, 2012).…”

Myxozoa in Haeckels Shadow

“…Chen et al's fossils [49] might not, after all, be too far off the trajectory of animal evolution predicted by the notion of bilateral cnidarians with "ParaHoxozoa" [33], "Urmetazoa" [50] or "Planulozoa" [51] as a clade of Placozoa, Cnidaria and Bilateria with Ctenophora its sister group [52].…”

“…If something as supposedly primitive as a ctenophore tissue is not related molecularly to bilaterian tissue, are biologists to drop the concept of tissue or redefine it in more inclusive terms? Furthermore, the absence of HOX genes would seem to deny ctenophores' claim for a genuine anterior-posterior axis [33]. Must new definitions also be applied to concepts of symmetry?…”

“…These cells are also mounted on a basal lamella (a subcellular electron-lucent [lamina rara]) and a granular fibrillar dense outer and fibrillar mesoglea [33][34][35].…”