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 lineage-specific 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.
Highlights
Nemerteans and phoronids are closely related lophotrochozoans—a group of animals including leeches, snails and other invertebrates
Genes expressed in lophophores of phoronids and brachiopods are strikingly similar to those employed in vertebrate head formation, novel genes, expanded gene families and redeployment of developmental genes contribute to the unique molecular identity of lophophores
With the support of deep RNA sequencing (RNA-seq) data obtained from 21 libraries, including embryonic stages and adult tissues, we estimated that the Notospermus and Phoronis genomes contain 43,294 and 20,473 protein-coding genes, respectively (Supplementary Fig. 5 and Supplementary Tables 4 and 5)
Summary
Nemerteans (ribbon worms) and phoronids (horseshoe worms) are closely related lophotrochozoans—a group of animals including leeches, snails and other invertebrates. Recent genomic studies have further shown that annelids and molluscs share various genomic features, such as gene family size and conserved orthologous gene clusters, with invertebrate deuterostomes (for example, amphioxus and sea urchins)[9] This observation raises the question of whether lophotrochozoans share some bilaterian ancestral features with invertebrate deuterostomes, which apparently have been lost in ecdysozoans and other lineages during protostome evolution. We present genomes of the nemertean Notospermus geniculatus and the phoronid Phoronis australis and explore lophotrochozoan evolution using comparative genomics With both genomic and transcriptomic data, our phylogenetic analyses provide evidence that nemerteans are probably sisters to lophophorates—a clade of animals with horseshoe-shaped lophophores comprising. Our study reveals the dual nature of lophotrochozoan genomes, showing both conservative and innovative characteristics during their evolution
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