Knowledge of the early evolution of fish largely depends on soft-bodied material from the Lower (Series 2) Cambrian period of South China1,2. Owing to the rarity of some of these forms and a general lack of comparative material from other deposits, interpretations of various features remain controversial3,4, as do their wider relationships amongst post-Cambrian early un-skeletonized jawless vertebrates. Here we redescribe Metaspriggina5 on the basis of new material from the Burgess Shale and exceptionally preserved material collected near Marble Canyon, British Columbia6, and three other Cambrian Burgess Shale-type deposits from Laurentia. This primitive fish displays unambiguous vertebrate features: a notochord, a pair of prominent camera-type eyes, paired nasal sacs, possible cranium and arcualia, W-shaped myomeres, and a post-anal tail. A striking feature is the branchial area with an array of bipartite bars. Apart from the anterior-most bar, which appears to be slightly thicker, each is associated with externally located gills, possibly housed in pouches. Phylogenetic analysis places Metaspriggina as a basal vertebrate, apparently close to the Chengjiang taxa Haikouichthys1,2,3,4 and Myllokunmingia1, demonstrating also that this primitive group of fish was cosmopolitan during Lower–Middle Cambrian times (Series 2–3). However, the arrangement of the branchial region in Metaspriggina has wider implications for reconstructing the morphology of the primitive vertebrate. Each bipartite bar is identified as being respectively equivalent to an epibranchial and ceratobranchial. This configuration suggests that a bipartite arrangement is primitive and reinforces the view that the branchial basket of lampreys7 is probably derived. Other features of Metaspriggina, including the external position of the gills and possible absence of a gill opposite the more robust anterior-most bar, are characteristic of gnathostomes8 and so may be primitive within vertebrates.
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We thank T. Lacalli for comments on an earlier draft of the manuscript, J. Mallatt for an extensive series of critiques, and J. Hoyal-Cuthill and C. Aria for assistance with phylogenetic analyses. We also thank M. Collins for technical drawings and reconstructions, and R. Thomas and M. Webster for information on the Kinzers and Parker formations, respectively. S.C.M. thanks V. Brown for manuscript preparation, and the Department of Earth Sciences and St John’s College, Cambridge for support. We thank Parks Canada for granting a collection and research permit to J.-B.C. (YNP-2012-12054). Fieldwork support for the 2012 expedition comes from the Royal Ontario Museum (DMV Research and Acquisition Fund and DNH Fieldwork Fund), M. Streng (Uppsala University and the Swedish Research Council), R. Gaines (Pomona College), G. Mangáno (University of Saskatchewan) and a Natural Sciences and Engineering Research Council Discovery Grant (to J.-B.C., #341944). This is Royal Ontario Museum Burgess Shale project number 53.
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BMC Evolutionary Biology (2016)