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A fossil of an aplacophoran from the Silurian of Herefordshire, England, is shown to have armour plating, supporting recent studies that have allied the worm-like, shell-less Aplacophora with the multi-shelled Polyplacophora, or chitons. The interrelationships of the Mollusca — one of the most diverse and species-rich animal phyla — have been contentious. Recent molecular work has allied the wormlike, shell-less Aplacophora with the multi-shelled Polyplacophora, or chitons. This is now corroborated with fossil evidence: the fossil of an aplacophoran from the Silurian of Herefordshire displays armour plating, suggesting a close link with chitons. The Mollusca is one of the most diverse, important and well-studied invertebrate phyla; however, relationships among major molluscan taxa have long been a subject of controversy1,2,3,4,5,6,7,8,9. In particular, the position of the shell-less vermiform Aplacophora and its relationship to the better-known Polyplacophora (chitons) have been problematic: Aplacophora has been treated as a paraphyletic or monophyletic group at the base of the Mollusca3,6,8, proximate to other derived clades such as Cephalopoda2,3,10, or as sister group to the Polyplacophora, forming the clade Aculifera1,5,7,11,12. Resolution of this debate is required to allow the evolutionary origins of Mollusca to be reconstructed with confidence. Recent fossil finds13,14,15,16 support the Aculifera hypothesis, demonstrating that the Palaeozoic-era palaeoloricate ‘chitons’ included taxa combining certain polyplacophoran and aplacophoran characteristics5. However, fossils combining an unambiguously aplacophoran-like body with chiton-like valves have remained elusive. Here we describe such a fossil, Kulindroplax perissokomos gen. et sp. nov., from the Herefordshire Lagerstatte17,18 (about 425 million years bp), a Silurian deposit preserving a marine biota18 in unusual three-dimensional detail. The specimen is reconstructed three-dimensionally through physical–optical tomography19. Phylogenetic analysis indicates that this and many other palaeoloricate chitons are crown-group aplacophorans.

Odontogriphus omalus was originally described as a problematic non-biomineralized lophophorate organism. Here we re-interpret Odontogriphus based on 189 new specimens including numerous exceptionally well preserved individuals from the Burgess Shale collections of the Royal Ontario Museum. This additional material provides compelling evidence that the feeding apparatus in Odontogriphus is a radula of molluscan architecture comprising two primary bipartite tooth rows attached to a radular membrane and showing replacement by posterior addition. Further characters supporting molluscan affinity include a broad foot bordered by numerous ctenidia located in a mantle groove and a stiffened cuticular dorsum. Odontogriphus has a radula similar to Wiwaxia corrugata but lacks a scleritome. We interpret these animals to be members of an early stem-group mollusc lineage that probably originated in the Neoproterozoic Ediacaran Period, providing support for the retention of a biomat-based grazing community from the late Precambrian Period until at least the Middle Cambrian.

Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera) or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites or can be shell-less but with a typical molluscan radula and serially repeated gills. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.

Evolutionary relationships among the eight major lineages of Mollusca have remained unresolved despite their diversity and importance. Previous investigations of molluscan phylogeny, based primarily on nuclear ribosomal gene sequences1–3 or morphological data4, have been unsuccessful at elucidating these relationships. Recently, phylogenomic studies using dozens to hundreds of genes have greatly improved our understanding of deep animal relationships5. However, limited genomic resources spanning molluscan diversity has prevented use of a phylogenomic approach. Here we use transcriptome and genome data from all major lineages (except Monoplacophora) and recover a well-supported topology for Mollusca. Our results strongly support the Aculifera hypothesis placing Polyplacophora (chitons) in a clade with a monophyletic Aplacophora (worm-like molluscs). Additionally, within Conchifera, a sister-taxon relationship between Gastropoda and Bivalvia is supported. This grouping has received little consideration and contains most (>95%) molluscan species. Thus we propose the node-based name Pleistomollusca. In light of these results, we examined the evolution of morphological characters and found support for advanced cephalization and shells as possibly having multiple origins within Mollusca.

Studies of the origin and radiation of the molluscs have yet to resolve many issues regarding their nearest relatives, phylogeny and ancestral characters1,2,3,4,5,6,7,8,9,10,11. The Polyplacophora (chitons) and the Aplacophora are widely interpreted as the most primitive extant molluscs2,3,9,10, but Lower Palaeozoic fossils of the former lack soft parts, and the latter were hitherto unrecognized as fossils. The Herefordshire Lagerstatte12 is a Silurian (about 425 Myr bp) deposit that preserves a marine biota in remarkable three-dimensional detail. The external surface of even non-biomineralized cuticle was preserved by entombment in volcanic ash, subsequent incorporation into concretions, and infilling of the fossils with sparry calcite13. Here we describe, from this deposit, a complete vermiform mollusc, which we interpret as a plated aplacophoran. Serial grinding at intervals of tens of micrometres, combined with computer-based reconstruction methods, renders the fossils in the round14.

PRESENT-DAY authorities agree that, within the Mollusca, the chitons (or Polyplacophora) are closely related to the solenogastres (or Aplacophora). An important item influencing this view is the description, by Pruvot1, of the development of seven overlapping, dorsal, plate-like spicules in the metamorphosing larva of the solenogastre, Nematomenia banyulensis. The appearance of these spicules has been considered to be a reminiscence of a chiton-like ancestor and, no doubt, has influenced many authors in coming to the conclusion that the solenogastres are degenerate chitons. Pruvot's description was based on observations on a single larva, but nonetheless the figure he gave of this developmental stage has been widely reproduced in general works.