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The extraordinary diversity in molluscan body plans, and the genomic mechanisms that enable it, remains one of the great questions of evolution. The eight distinct living taxonomic classes of molluscs are each unambiguously monophyletic; however, significant controversy remains about the phylogenetic relationships among those eight branches. Molluscs are the second-largest animal phylum, with over 100 000 living species with broad biological, economic and medical interest. To date, only around 53 genome assemblies have been accessioned to NCBI GenBank covering only four of the eight living molluscan classes. Furthermore, the molluscan taxa where partial or whole-genome assemblies are available are often aberrantly fast evolving or recently derived lineages. Characteristic adaptations provide interesting targets for whole-genome projects, in animals like the scaly-foot snail or octopus, but without basal-branching lineages for comparison, the context of recently derived features cannot be assessed. The currently available genomes also create a non-optimal set of taxa for resolving deeper phylogenetic branches: they are a small sample representing a large group, and those that are available come primarily from a rarefied pool. Thoughtful selection of taxa for future projects should focus on the blank areas of the molluscan tree, which are ripe with opportunities to delve into peculiarities of genome evolution, and reveal the biology and evolutionary history of molluscs. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.

The Scaly-foot Snail, Chrysomallon squamiferum , presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanisms underlying the evolutionary diversification of biomineralised armour. Here, we present a high-quality whole-genome assembly and tissue-specific transcriptomic data, and show that scale and shell formation in the Scaly-foot Snail employ independent subsets of 25 highly-expressed transcription factors. Comparisons with other lophotrochozoan genomes imply that this biomineralisation toolkit is ancient, though expression patterns differ across major lineages. We suggest that the ability of lophotrochozoan lineages to generate a wide range of hard parts, exemplified by the remarkable morphological disparity in Mollusca, draws on a capacity for dynamic modification of the expression and positioning of toolkit elements across the genome. The Scaly-foot Snail, Chrysomallon squamiferum , is a model for understanding the evolution of biomineralised armour. Here, the authors present a chromosome-level reference genome assembly and tissue-specific transcriptomic data for this enigmatic organism.

Mollusca is the second most species-rich animal phylum, but the pathways of early molluscan evolution have long been controversial 1 , 2 , 3 , 4 – 5 . Modern faunas retain only a fraction of the past forms in this hyperdiverse and long-lived group. Recent analyses 6 , 7 – 8 have consistently recovered a fundamental split into two sister clades, Conchifera (including gastropods, bivalves and cephalopods) and Aculifera 9 , comprising Polyplacophora (‘chitons’) and Aplacophora. Molluscan evolution in toto is characterized by plasticity in body-plan characters 10 , but historically aculiferans have been interpreted as more conservative 10 , 11 . The few completely preserved aculiferan or aculiferan-like fossils from the early Palaeozoic 12 , 13 , 14 , 15 , 16 , 17 , 18 – 19 have been largely regarded as transitional forms that inform questions of character polarity between the extant polyplacophoran and aplacophoran body forms 20 , 21 . The history of early aculiferans, and the morphological and ecological range that they occupied, remain inadequately sampled. Here we describe two new three-dimensionally preserved aculiferan species from the Silurian Herefordshire Lagerstätte 22 , 23 , which substantially extend the morphological and ecological range of the clade. Phylogenetic analyses indicate positions within a complex nexus of taxa and suggest reversals in the states of fundamental characters such as the presence of valves and the nature of the foot. In contrast to previous hypotheses of morphological conservatism, evolution in early aculiferans generated a profusion of unusual forms comparable to the diversification of other crown-group molluscs. Fossils of two new worm-like aculiferan species add to the diversity of this group, showing that evolution in early aculiferans generated unusual forms comparable to other crown-group molluscs.

A major question in animal evolution is how genotypic and phenotypic changes are related, and another is when and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades, and an updated phylogeny for the phylum. We constructed 20 ancient molluscan linkage groups (MLGs) and show that these are relatively conserved in bivalve karyotypes, but in chitons they are subject to re-ordering, rearrangement, fusion, or partial duplication and vary even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.

Background The Peruvian ‘chanque’ or Chilean ‘loco’ Concholepas concholepas is an economically, ecologically, and culturally important muricid gastropod heavily exploited by artisanal fisheries in the temperate southeastern Pacific Ocean. In this study, we have profited from a set of bioinformatics tools to recover important biological information of C. concholepas from low-coverage short-read NGS datasets. Specifically, we calculated the size of the nuclear genome, ploidy, and estimated transposable elements content using an in silico k-mer approach, we discovered, annotated, and quantified those transposable elements, we assembled and annotated the 45S rDNA RNA operon and mitochondrial genome, and we confirmed the phylogenetic position of C. concholepas within the muricid subfamily Rapaninae based on translated protein coding genes. Results Using a k-mer approach, the haploid genome size estimated for the predicted diploid genome of C. concholepas varied between 1.83 Gbp (with kmer = 24) and 2.32 Gbp (with kmer = 36). Between half and two thirds of the nuclear genome of C. concholepas was composed of transposable elements. The most common transposable elements were classified as Long Interspersed Nuclear Elements and Short Interspersed Nuclear Elements, which were more abundant than DNA transposons, simple repeats, and Long Terminal Repeats. Less abundant repeat elements included Helitron mobile elements, 45S rRNA DNA, and Satellite DNA, among a few others.The 45S rRNA DNA operon of C. concholepas that encodes for the ssrRNA, 5.8S rRNA, and lsrRNA genes was assembled into a single contig 8,090 bp long. The assembled mitochondrial genome of C. concholepas is 15,449 bp long and encodes 13 protein coding genes, two ribosomal genes, and 22 transfer RNAs. Conclusion The information gained by this study will inform the assembly of a high quality nuclear genome for C. concholepas and will support bioprospecting and biomonitoring using environmental DNA to advance development of conservation and management plans in this overexploited marine snail.

Background In this study, we present the first chromosome-scale genome of Verpa penis (Linnaeus, 1758), and the first for the bivalve clade Anomalodesmata. The present study has two separate foci. Primarily, we provide the genetic resource to bridge further studies from genome to phenome and propose hypotheses to guide future empirical investigations. Secondarily, based on morphology, we outline a conceptual exploration to address their adaptation. Watering-pot shells have been called “the weirdest bivalves” for their fused tubular shell resembling the spout of a watering can. This adventitious tube arose twice convergently in clavagelloidean bivalves. However, previous literature has never provided a convincing adaptive pathway. Results The genome assembly of V. penis was about 507 Mb, with contig N50 of 5.33 Mb, and has 96.5% of sequences anchored onto 19 pseudochromosomes. Phylogenomic analyses of this new genome in context of other bivalves confirms the placement for Anomalodesmata as sister to the clade Imparidentia. Contrary to expectations from its highly modified body plan, there is no evidence of chromosome reduction compared to the ancestral karyotype of heterodont bivalves (1  N  = 19). Drawing on established principles from engineering as well as morphology, the thought experiment about the adventitious tube seeks to extend current understanding by exploring parallels with other built structures. A new hypothesis explains one possible interpretation of the adaptive significance of this body form: it is potentially structurally optimised for vertical stability in relatively soft sediments, with parallels to the engineering principles of a suction anchor. Conclusions While the conclusions presented here on morphological interpretations are theoretical, this serves as a foundation for further empirical validation and refinement. Our study offers new insights to a long-standing mystery in molluscan body forms and provides genomic resources that are relevant to understanding molluscan evolution, biomineralisation, and biomimetic design.

Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flow in ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics.

Trails, burrows, and other “life traces” in sediment provide important evidence for understanding ecology—both of the maker and of other users—and behavioral information often lacking in inaccessible ecosystems, such as the deep sea or those that are already extinct. Here, we report novel sublinear rows of openings in the abyssal plains of the North Pacific, and the first plausible hypothesis for a maker of these constructions. Enigmatic serial burrows have now been recorded in the Pacific and Atlantic deep sea. Based on image and specimen evidence, we propose that these Bering Sea excavations represent amphipod burrows, while the maker of the previously known Mid-Atlantic Ridge constructions remains undetermined. We propose that maerid amphipods could create the Pacific burrows by eating–digging horizontally below the surface along a nutrient-rich layer in the sediment, making the serial openings above them as they go, for conveniently removing excavated sediment as the excavation progresses. These striking structures contribute to local biodiversity, and their maker could be considered a deep-sea ecosystem engineer.

Background Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta , from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the ‘scaly-foot gastropod’ Chrysomallon squamiferum . Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs. Results Transmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta , as also seen in Chrysomallon . They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon , which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon , Gigantopelta possesses true ganglia and is gonochoristic. Conclusions Key anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont’s adaptations to an extreme environment, are driven by optimising bacteria’s access to vent nutrients. By comparing Gigantopelta and Chrysomallon , we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.