Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

Abstract

*Nemerteans (ribbon worms) and phoronids (horseshoe worms) are closely related lophotrochozoans-a group of animals including leeches, snails and other invertebrates. Lophotrochozoans represent a superphylum that is crucial to our understanding of bilaterian evolution. However, given the inconsistency of molecular and morphological data for these groups, their origins have been unclear. Here, we present draft genomes of the nemertean Notospermus geniculatus and the phoronid Phoronis australis, together with transcriptomes along the adult bodies. Our genome-based phylogenetic analyses place Nemertea sister to the group containing Phoronida and Brachiopoda. We show that lophotrochozoans share many gene families with deuterostomes, suggesting that these two groups retain a core bilaterian gene repertoire that ecdysozoans (for example, flies and nematodes) and platyzoans (for example, flatworms and rotifers) do not. Comparative transcriptomics demonstrates that lophophores of phoronids and brachiopods are similar not only morphologically, but also at the molecular level. Despite dissimilar head structures, lophophores express vertebrate head and neuronal marker genes. This finding suggests a common origin of bilaterian head patterning, although different heads evolved independently in each lineage. Furthermore, we observe lineagespecific expansions of innate immunity and toxin-related genes. Together, our study reveals a dual nature of lophotrochozoans, where conserved and lineage-specific features shape their evolution. Articles NaTure eCOLOgy & evOLuTiONphoronids, ectoprocts and brachiopods, although the position of ectoprocts is questionable under a sensitivity analysis. Our results clearly show that lophotrochozoans have a different evolutionary history than other spiralians (or platyzoans), such as flatworms and rotifers. In particular, lophotrochozoans retain a basic bilaterian gene repertoire, which is probably lost in ecdysozoans and other spiralian lineages. Unexpectedly, genes specifically expressed in lophophores of phoronids and brachiopods are strikingly similar to those employed in vertebrate head formation, although novel genes, expanded gene families and redeployment of developmental genes also contribute to the unique molecular identity of lophophores. Furthermore, we provide examples of lineage-specific genomic features in lophotrochozoans, such as the expansion of innate immunity and toxin-related genes. Taken together, our study reveals the dual nature of lophotrochozoan genomes, showing both conservative and innovative characteristics during their evolution.

A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

“…The topology of the cladogram is adapted from data in Weigert et al. (2014) and Luo et al. (2018), and the position of some gain/loss events from Paps et al.…”

“…This may be an artefact of the query set used by each study, indicating the paramount importance of a diverse, constantly updated, and recursive query pool, and of repeating searches of previously surveyed genomes to make use of expansions to the query pool. In addition, there is a need for ever greater taxon sampling, including undersampled annelid (e.g., Amphinomidae [Mehr et al 2015]) and mollusc (e.g., Cephalopoda [Albertin et al 2015]) clades, and the recently published nemertean and phoronid draft genomes (Luo et al 2018). …”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…This is in contrast to brachiopods, the putative close relatives of Phoronida, where various level of Hox cluster disorganization is shown ( Fig. 1A) and temporal and spatial collinearity is missing (16,40,89,90). Therefore, it remains important to examine whether phoronid Hox genes are also expressed in the spatio-temporally collinear manner during development, which would correspond with the retention of the organized Hox cluster shown in this clade.…”

“…details of its life cycle (C). Hox cluster organization and Hox gene complement in A are taken from (16,89,91).…”

“…Our aim was to answer whether phoronid Hox genes show staggered expression along the A-P axis at any of the developmental stages as well as to examine if there are traces of temporal collinearity that could hint to the presence of a Hox cluster as described for another phoronid Ph. australis (89). We also wanted to investigate whether there are differences in the Hox gene expression (and possibly in the patterning of the A-P axes) between the larva and the rudiment of the forming juvenile worm and compare our findings with other species that exhibit extreme metamorphosis.…”