A new interpretation of Pikaia reveals the origins of the chordate body plan

Our understanding of the evolutionary origin of Chordata, one of the most disparate and ecologically significant animal phyla, is hindered by a lack of unambiguous stem-group relatives. Problematic Cambrian fossils that have been considered as candidate chordates include vetulicolians,1Gee H. On being vetulicolian.Nature. 2001; 414: 407-409Crossref PubMed Scopus (27) Google Scholar Yunnanozoon,2Chen J.Y. Dzik J. Edgecombe G.D. Ramsköld L. Zhou G.Q. A possible Early Cambrian chordate.Nature. 1995; 377: 720-722Crossref Google Scholar and the iconic Pikaia.3Conway Morris S. Caron J.B. Pikaia gracilens Walcott, a stem-group chordate from the Middle Cambrian of British Columbia.Biol. Rev. 2012; 87: 480-512Crossref PubMed Scopus (0) Google Scholar However, their phylogenetic placement has remained poorly constrained, impeding reconstructions of character evolution along the chordate stem lineage. Here we reinterpret the morphology of Pikaia, providing evidence for a gut canal and, crucially, a dorsal nerve cord—a robust chordate synapomorphy. The identification of these structures underpins a new anatomical model of Pikaia that shows that this fossil was previously interpreted upside down. We reveal a myomere configuration intermediate between amphioxus and vertebrates and establish morphological links between Yunnanozoon, Pikaia, and uncontroversial chordates. In this light, we perform a new phylogenetic analysis, using a revised, comprehensive deuterostome dataset, and establish a chordate stem lineage. We resolve vetulicolians as a paraphyletic group comprising the earliest diverging stem chordates, subtending a grade of more derived stem-group chordates comprising Yunnanozoon and Pikaia. Our phylogenetic results reveal the stepwise acquisition of characters diagnostic of the chordate crown group. In addition, they chart a phase in early chordate evolution defined by the gradual integration of the pharyngeal region with a segmented axial musculature, supporting classical evolutionary-developmental hypotheses of chordate origins4Romer A.S. The vertebrate as a dual animal—somatic and visceral.in: Evolutionary Biology. Springer, 1972: 121-156Crossref Google Scholar and revealing a "lost chapter" in the history of the phylum.