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The almost simultaneous emergence of major animal phyla during the early Cambrian shaped modern animal biodiversity. Reconstructing evolutionary relationships among such closely spaced branches in the animal tree of life has proven to be a major challenge, hindering understanding of early animal evolution and the fossil record. This is particularly true in the species-rich and highly varied Mollusca where dramatic inconsistency among paleontological, morphological, and molecular evidence has led to a long-standing debate about the group’s phylogeny and the nature of dozens of enigmatic fossil taxa. A critical step needed to overcome this issue is to supplement available genomic data, which is plentiful for well-studied lineages, with genomes from rare but key lineages, such as Scaphopoda. Here, by presenting chromosome-level genomes from both extant scaphopod orders and leveraging complete genomes spanning Mollusca, we provide strong support for Scaphopoda as the sister taxon of Bivalvia, revitalizing the morphology-based Diasoma hypothesis originally proposed 50 years ago. Our molecular clock analysis confidently dates the split between Bivalvia and Scaphopoda at ~520 Ma, prompting a reinterpretation of controversial laterally compressed Early Cambrian fossils, includingAnabarella,Watsonella,andMellopegma,as stem diasomes. Moreover, we show that incongruence in the phylogenetic placement of Scaphopoda in previous phylogenomic studies was due to ancient incomplete lineage sorting (ILS) that occurred during the rapid radiation of Conchifera. Our findings highlight the need to consider ILS as a potential source of error in deep phylogeny reconstruction, especially in the context of the unique nature of the Cambrian Explosion. 

Abstract The extraordinary window of phosphatized and phosphatic small shelly fossils (SSF) during the early and middle Cambrian is an important testament to the radiation of biomineralizing metazoans. WhileSSFare well known from most Cambrian palaeocontinents during this time interval, western Laurentia has relatively fewSSFfaunas. Here we describe a diverseSSFfauna from the early Cambrian (Stages 3–4) Mural Formation at three localities in Alberta and British Columbia, Canada, complemented by carbon isotope measurements to aid in a potential future bio‐chemostratigraphic framework. The fauna expands the recordedSSFassemblage diversity in western Laurentia and includes several brachiopods, four bradoriids, three chancelloriids, two hyoliths, a tommotiid and a helcionellid mollusc as well as echinoderm ossicles and specimens ofMicrodictyon,VolborthellaandHyolithellus. New taxa include the tommotiid genusCanadiellagen. nov., the new bradoriid speciesHipponicharion perforatasp. nov. andPseudobeyrichona tauratasp. nov. Compared with contemporaneous faunas from western Laurentia, the fauna is relatively diverse, particularly in taxa with originally phosphatic shells, which appear to be associated with archaeocyathid build‐ups. This suggests that the generally low faunal diversity in western Laurentia may be at least partly a consequence of poor sampling of suitable archaeocyathan reef environments. In addition, the tommotiidCanadiella filigranaappears to be of biostratigraphical significance in Cambrian Stage 3 strata of western Laurentia, and the unexpected high diversity of bradoriid arthropods in the fauna also suggests that this group may prove useful for biostratigraphical resolution in the region.