The big, the small and the weird: A phylogenomic analysis of extant Priapulida

Abstract

Priapulida is a small phylum of 22 described species that are divided into two size classes (microscopic and macroscopic), distinguished by adult and larval morphology. Most priapulidans are rare or live in inaccessible habitats, and freshly collected material for molecular studies is difficult to obtain. With this study, we for the first time aim to resolve the phylogeny of extant Priapulida using transcriptomic, genomic, and morphological data. We analyze six newly assembled transcriptomes alongside existing data, covering seven species and four genera. Additionally, we include genomic data from museum-preserved species, adding another genus via low-coverage genome sequencing. Conserved regions from these data produce a combined phylogenomic tree, augmented by morphological data to suggest positions for the rare taxa Acanthopriapulus and Maccabeus. Our findings show that the microscopic Meiopriapulus consistently groups as a sister taxon to other priapulidans and not with Tubiluchus, as suggested in previous studies. Maccabeus, which exhibits both size-class characteristics, is the sister taxon to all the macroscopic species, while Acanthopriapulus is a sister taxon to Priapulus, but molecular data are needed to support their suggested positions. Ancestral state reconstruction suggests that small body size, lack of caudal appendages, and internal fertilization are ancestral traits for Priapulida. This supports the derived evolution of macroscopic size and other traits in the group, aligning with its microscopic sister groups Kinorhyncha and Loricifera. Due to the diversity of priapulidans and the unique morphologies of some species, further fossil studies and potential discoveries of priapulidan microfossils are essential to fully understand the evolutionary history of this phylum.