Tunicate tails, stolons, and the origin of the vertebrate trunk

Abstract

Tunicates are primitive chordates that develop a transient ‘tail’ in the larval stage that is generally interpreted as a rudimentary version of the vertebrate trunk. Not all tunicates have tails, however. The groups that lack them, salps and pyrosomes, instead have a trunk-like reproductive stolon located approximately where the tail would otherwise be. In salps, files of blastozooids are formed along the sides of the stolon. The tail and caudal trunk in more advanced chordates could have evolved from a stolon of this type, an idea referred to here as the ‘stolon hypothesis’. This means the vertebrate body could be a composite structure, since there is the potential for each somite to incorporate elements originally derived from a complete functional zooid. If indeed this has occurred, it should be reflected in some fashion in gene expression patterns in the vertebrate trunk. Selected morphological and molecular data are reviewed to show that they provide some circumstantial support for the stolon hypothesis. The case would be stronger if it could be demonstrated that salps and/or pyrosomes are ancestral to other tunicates. The molecular phylogenies so far available generally support the idea of a pelagic ancestor, but offer only limited guidance as to which of the surviving pelagic groups most closely resembles it. The principal testable prediction of the stolon hypothesis is that head structures (or their homologues) should be duplicated in series in the trunk in advanced chordates, and vice versa, i.e. trunk structures should occur in the head. The distribution of both rhabdomeric photoreceptors and nephridia in amphioxus conform with this prediction. Equally striking is the involvement of the Pax2 gene in the development of both the inner ear and nephric ducts in vertebrates. The stolon hypothesis would explain this as a consequence of the common origin of otic capsules and excretory ducts from atrial rudiments: from the paired rudiments of the parent oozooid in the case of the otic capsule (these express Pax2 according to recent ascidian data), and from tubular rudiments in the stolon in the case of the excretory ducts.