The ctenophore genome and the evolutionary origins of neural systems

Abstract

The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores, or comb jellies, have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here, we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well-recognized in ctenophores, many bilaterian neuron-specific genes and genes of “classical” neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.

Genomic data do not support comb jellies as the sister group to all other animals

“…Although statistical support for this branching order is very low (Fig. S2A), the same is true for the tree found by Moroz et al (5). Finally, an analysis of this dataset using the better-fitting site-heterogeneous CAT-GTR model (45) supported demosponges, glass sponges, and homoscleromorphs as the sister group of all other animals, followed by ctenophores.…”

“…In the Pleurobrachia bachei genome study (5), the Ctenophora-sister hypothesis was obtained from the analysis of two datasets, one of which was constructed to maximize the number of species and the other to maximize the number of proteins. Whereas the dataset emphasizing protein sampling was broadly comparable to the dataset of Ryan et al (4), the dataset emphasizing species sampling (Moroz-3D; Methods) was unique because it included the largest number of ctenophores sampled thus far.…”

“…Although results from the first study supporting Ctenophorasister (2) were questioned soon thereafter and suggested to be an artifact stemming from the inclusion of too few nonbilaterian species (12) and the use of too rapidly evolving genes (13), this hypothesis has recently been revived in several studies, including analyses of the first two complete ctenophore nuclear genomes, as well as transcriptomic datasets from numerous other ctenophore species (4)(5)(6). Here, we present analyses of key datasets from Ryan et al (4), Moroz et al (5), and Whelan et al (6), and identify several problems in these studies, specifically the combined use of relatively simplistic models of molecular…”

“…Here, we present analyses of key datasets from Ryan et al (4), Moroz et al (5), and Whelan et al (6), and identify several problems in these studies, specifically the combined use of relatively simplistic models of molecular…”

Re-evaluating the phylogeny of Sipuncula through transcriptomics

“…Nextgeneration sequencing (NGS) now enables us to generate large data sets for many species at a relatively low cost. The systematic community has necessarily progressed from candidate genes through EST-based methods to 454 and Illumina-based transcriptome and genome datasets to resolve major relationships among the animal phyla (e.g., Dunn et al, 2008;Hejnol et al, 2009;Nosenko et al, 2013;Ryan et al, 2013;Moroz et al, 2014). Long outstanding issues have been resolved for within-phylum relationships among arthropods, molluscs, and annelids, to mention just some of the largest animal phyla (e.g., Meusemann et al, 2010;Kocot et al, 2011;Smith et al, 2011;Struck et al, 2011;von Reumont et al, 2012;Andrade et al, 2014;Weigert et al, 2014).…”