The cellular basis of photobehavior in the tufted parenchymella larva of demosponges

The mechanisms by which light elicits a phototactic response in sponge larvae remain poorly understood. Here we investigate histological and behavioral aspects of the photoresponse in parenchymella larvae of three demosponges. Two species are photonegative during their entire larval life, while the other, initially photopositive, becomes photonegative only after swimming in the laboratory for 4 h to 6 h. All larvae are bullet-shaped, with a uniformly ciliated surface, except at their posterior end, which is unciliated but surrounded by a distinctive ring of long cilia, the tuft. The short cilia beat metachronally, generating the thrust to move the larva forward with clockwise rotation. The lone cilia of the tuft do not beat metachronally and are apparently more involved in maneuvering than in the generation of thrust. Transmission electron microscopy revealed in one species that the axoneme of the short cilia contains a distinctive 9x3+2 microtubule pattern at its base, but the presence of such an arrangement in cilia of the tuft remains uncorroborated. Nevertheless, the differences in beating characteristics between the monociliated cells of the tuft and those in the rest of the body correspond to other cytological differences. Cilia of the tuft have a type-l basal body, a large basal foot, and a branched rootlet, whereas the remaining cilia have a type-II basal body, a smaller and simpler basal foot, and an unbranched rootlet. Furthermore, the cells forming the tuft have a characteristic distal protrusion filled with pigments and mitochondria. Several of these traits suggest that the monociliated cells of the tuft are involved in the larval photoresponse both as sensors and effectors. Drastic changes in light intensity have no effect on the beating of the short cilia. In contrast, they cause a predictable and instantaneous movement of each cilium in the tuft, triggering expansions and contractions of either a part or the entire tuft, which in turn alters the direction of swimming. Observations on free-swimming larvae suggest that the tuft works as a passive light-sensitive rudder in both photonegative species that contract their posterior cilia under high irradiance and in photopositive species that expand their cilia under high irradiance. However, in photonegative larvae that expand the tuft under high irradiance, an active ciliary coordination by the larva needs to be invoked to explain a deviation of the swimming trajectory.