Ciliated larvae turn spiny: novelties in the miniaturized miracidium of Bunocotyle progenetica (Digenea: Hemiuroidea)

Abstract Background Miracidia, the larvae of digeneans, infect a molluscan host. In many species they are ciliated swimmers that actively locate a snail. In several digenean lineages, however, the miracidia are miniaturized and enter molluscs passively, being swallowed. The contrast between active and passive miracidia is sharp, and the latter are typically simplified and feature morphological novelties. In the Hemiurata group, miracidia show reduced ciliation and have evolved surface spines. An extreme example is the miracidium of Bunocotyle progenetica , whose entire body is covered with spines. Larval ciliation is considered one of the key features of Neodermata, yet it is lost in B. progenetica . How could such a transformation have occurred? Results Using serial transmission electron microscopy, we show that the miracidium of B. progenetica is covered by three spiny epithelial plates. Each spine is supported by an elongated intracellular structure similar to the striated rootlet of a cilium. All organ systems of the miracidium are markedly reduced relative to those of non-miniaturized miracidia. Experimental infection of the snail host revealed that the miracidium sheds its epithelial plates upon metamorphosis and transforms into a sporocyst, which migrates to the snail heart. The sporocyst surface arises through eversion of the peculiar membranous channels of the neodermis. Apart from this transformation of the body wall, metamorphosis involves few structural changes. Over the first two weeks, the mother sporocyst triples in size, increasing the number of muscle cells and neodermis cytons, likely through stem-cell division and differentiation. Snail haemocytes appear to respond to the infection and contact the sporocyst, forming short extracellular bridges. Conclusions Miniaturization accompanied by a shift in infection strategy has driven the emergence of structural novelties in miracidia. In B. progenetica , spines have replaced surface cilia, co-opting the ciliary striated rootlet as a structural scaffold. Although the miracidium of B. progenetica is greatly simplified relative to non-miniaturized miracidia, its mother sporocyst restores somatic complexity and develops into worms comparable to those of other digeneans.