Metamorphic remodeling of morphology and the body cavity in Phoronopsis harmeri (Lophotrochozoa, Phoronida): the evolution of the phoronid body plan and life cycle

BACKGROUND: Phoronids undergo a remarkable metamorphosis, in which some parts of the larval body are consumed by the juvenile and the body plan completely changes. According to the only previous hypothesis concerning the evolution of the phoronid body plan, a hypothetical ancestor of phoronids inhabited a U-shaped burrow in soft sediment, where it drew the anterior and posterior parts of the body together and eventually fused them. In the current study, we investigated the metamorphosis of Phoronopsis harmeri with light, electron, and laser confocal microscopy. RESULTS: During metamorphosis, the larval hood is engulfed by the juvenile; the epidermis of the postroral ciliated band is squeezed from the tentacular epidermis and then engulfed; the larval telotroch undergoes cell death and disappears; and the juvenile body forms from the metasomal sack of the larva. The dorsal side of the larva becomes very short, whereas the ventral side becomes very long. The terminal portion of the juvenile body is the ampulla, which can repeatedly increase and decrease in diameter. This flexibility of the ampulla enables the juvenile to dig into the sediment. The large blastocoel of the larval collar gives rise to the lophophoral blood vessels of the juvenile. The dorsal blood vessel of the larva becomes the definitive median blood vessel. The juvenile inherits the larval protocoel, mesocoel, and metacoel. Late in metamorphosis, however, the protocoel loses its epithelial structure: the desmosomes between cells and the basal lamina under the cells disappear. This loss may reflect a reduction of the protocoel, which is a characteristic of some recent phoronids. CONCLUSIONS: Based on our investigation of P. harmeri metamorphosis, we hypothesize that the phoronid ancestor was worm-like animal that possessed preoral, tentacular, and trunk coeloms. It lived on the soft sediment and collected food with its tentacles. When threatened, this worm-like ancestor buried itself in the soft sediment by means of the ventral protrusion into which the loop of the intestine and the blood vessels were drawn. We propose that this behavior gave rise to the body plan of all recent phoronids. The evolution of phoronid life cycle seems having more in common with“intercalation” than “terminal addition” theories. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0504-0) contains supplementary material, which is available to authorized users.