New insights into the phylogeny of Neogastropoda aided by draft genome sequencing of a volutid snail

Abstract

Neogastropoda is a large order of predominantly marine gastropod molluscs, typically predatory or parasitic on other animals. It includes over 16,000 species representing a large post‐Cretaceous radiation, but the internal phylogenetic relationships of contained taxa are far from resolved, with inconsistent results from nuclear genes, mitogenomes, and morphology. One major issue in reconstructing the molecular phylogeny is the lack of high‐quality sequences for early‐diverging families and superfamilies such as Volutidae (Volutoidea). Here, we examine the superfamily‐level phylogenetic relationships in Neogastropoda, aided by newly sequenced draft genome and mitogenome of the volutid snail Fulgoraria chinoi from the deep sea off Japan. The genome of F. chinoi is relatively large at 1.54 Gb but exhibits low genome heterozygosity; over 54% of this genome constitutes of repeat contents, and we find evidence for active insertion of transposable elements, particularly LINEs and SINEs. A total of 50,792 protein‐coding genes (PCGs) were predicted from the nuclear genome, and a circular mitogenome was also assembled and annotated. Our phylogenetic analyses using mitogenomes recovered each neogastropod superfamily as monophyletic, though also revealed inconsistent phylogenetic signals within superfamilies. Phylogenetic reconstructions using the PCGs resulted in a robust tree from different models and data matrices, recovering Volutoidea as the earliest diverging superfamily (among those for which comparable data is available) within a monophyletic Neogastropoda. Dated phylogenetic analysis revealed an early Cretaceous radiation of Neogastropoda, congruent with the fossil record. Our study provides a robust internal evolutionary framework for the speciose but genomically undersampled Neogastropoda, and expands the available genomic resources for this order. Genomic data for key missing lineages such as Mitroidea, Olivoidea, and Cancellariidae are much sought in the future for a full understanding of Neogastropoda evolution.