Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

Abstract

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor-cell evolution in animals. The two cell types coexist in some animals, however how these cells functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming in non-directional UV light, a behavior absent in ciliary-opsin knockout larvae. UV avoidance overrides positive phototaxis mediated by the rhabdomeric eyes such that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during vertical migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptor cells in a zooplankton larva.

eLife digest

The animal kingdom contains many different types of eyes, but all share certain features in common. All detect light using specialized cells called photoreceptors, of which there are two main kinds: ciliary and rhabdomeric. Crustaceans and their relatives, including insects, have rhabdomeric photoreceptors; while animals with backbones, including humans, have ciliary photoreceptors. There are also several groups of animals, mostly sea-dwellers, that inherited both types of photoreceptors from their ancestors that lived millions of years ago. These include the marine ragworm, Platynereis dumerilii.

The larvae of Platynereis are free-swimming plankton. Each has a transparent brain and six small, pigmented eyes. The eyes contain rhabdomeric photoreceptors. These enable the larvae to detect and swim towards light sources. Yet the larval brain also contains ciliary photoreceptors, the role of which was unknown.

Verasztó, Gühmann et al. now show that ultraviolet light activates ciliary photoreceptors, whereas cyan, or blue-green, light inhibits them. Shining ultraviolet light onto Platynereis larvae makes the larvae swim downwards. By contrast, cyan light makes the larvae swim upwards. In the ocean, ultraviolet light is most intense near the surface, while cyan light reaches greater depths. Ciliary photoreceptors thus help Platynereis to avoid harmful ultraviolet radiation near the surface. Though if the larvae swim too deep, cyan light inhibits the ciliary photoreceptors and activates the rhabdomeric pigmented eyes. This makes the larvae swim upwards again.

Using high-powered microscopy, Verasztó, Gühmann et al. confirm that neural circuits containing ciliary photoreceptors exchange messages with circuits containing rhabdomeric photoreceptors. This suggests that the two work together to form a depth gauge. By enabling the larvae to swim at a preferred depth, the depth gauge influences where the worms end up as adults. Its discovery should also stimulate new ideas about the evolution of eyes and photoreceptors.