Abstract

Phototaxis is widespread among planktonic organisms, and can be found in the larval stages of sponges, cnidarians, protostomes and deuterostomes. The ability of zooplankton to find their preferred water depth depends on varying daily light conditions and developmental stage. Planktonic larvae often undergo a behavioral change, switching from positive phototaxis, characteristic of the post-hatching stages, to negative phototaxis, characteristic of later larval stages before settlement and metamorphosis. The marine annelid Platynereis dumerilii is an excellent laboratory model to study the mechanisms of larval phototaxis. Platynereis has a bentho-pelagic-life cycle with a pelagic larva that shows early positive and late negative phototaxis. The neuronal circuit and mechanism of early larval phototaxis is well understood: the larval eyespots, consisting of a shading pigment cell and a rhabdomeric photoreceptor cell, mediate this response. The eyespot photoreceptor directly innervates the ciliary band (prototroch). The mechanism and neural circuitry underlying negative phototaxis is unknown. To study the mechanism of negative phototaxis in Platynereis larvae we combined behavioral experiments, laser ablation, and transmission electron microscopy. Late Platynereis larvae have six eyes, the two eyespots and four additional dorsal eyes, precursors of the adult eyes. We characterized the role of these eyes in larval phototaxis, using laser ablations. Our electron microscopic reconstructions revealed how the eyes regulate motor output during phototactic turning. The Platynereis eye circuit shows the hallmarks of a simple visual system, including spatial light detection and contrast modulation, illustrating how image-forming eyes may have evolved via intermediate stages capable to contrast only a light and a dark pixel during phototaxis.