Mechanism of phototaxis in marine zooplankton

Abstract

The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell. They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution [1][2][3][4] . Eyespots cannot form images but enable the animal to sense the direction of light. They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light. Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton 5 , which is thought to represent the biggest biomass transport on Earth 6,7 . Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood. Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model 8 . We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow. Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light. The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation. These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it. We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes. We assayed phototaxis of Platynereis larvae (Fig. 1a, b) in a dark chamber with .750 nm transmission illumination. Larval swimming in a 13130.2 cm cuvette in the dark chamber was recorded after providing a directional diffuse white light stimulus at one end of the chamber (Supplementary Fig. 1 and Supplementary Movie 1). We measured the efficiency of phototaxis by calculating the average displacement of the larvae towards the light (Fig. 1c). Positive phototaxis started at 25 h of development and lasted for two days. The spectral sensitivity was broad (365-545 nm) with two maxima at 410 and 490 nm (Fig. 1d), similar to that of phototactic larvae from other species 9 . Phototaxis could be triggered with intensities .0.5 mW cm 22 using 500-nm monochromatic light. Phototactic larvae swim in a right-handed helix (that is, clockwise forward movement) of a diameter of 60-300 mm while rotating around their anterior-posterior axis with one full turn every 0.6-0.9 s. During swimming the dorsal side of the larva is always directed towards the axis of the helix so that a 360u axial rotation takes place in one pitch of the helix (Fig. 1e). This is a general phenomenon among protozoa and ciliated animal larvae [10][11][12][13][14] . Platynereis larvae develop a pair of eyespots consisting of a pigment cell and a rhabdomeric photore...

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

“…We observed that the branched axons are full of large dense-cored vesicles (Fig. 3H), but are completely devoid of synapses that are typical for cells containing classical neurotransmitters (45), indicating that these MIP chemosensory neurons signal exclusively via the release of neuropeptides.…”

“…4A). The activation was specific, as 12 other Platynereis neuropeptides (19,45) did not activate the MIP receptor (Fig. 4B).…”

First-order phase transition in a model of self-propelled particles with variable angular range of interaction

“…For example, the cyclopean field of view (i.e., combined field of view of both eyes [26]) of the grey-headed Albatross is about 270 • in the horizontal plane [27], and that of Dasyatis sabina fish is about 327 • in the horizontal plane [26]. This kind of restricted view of the neighborhood also plays a role in the phototactic motion of certain marine organisms such as Platynereis larvae [28]. Thus exploration of the effects of limitation of the angular range of interaction neighborhood should be of interest in the study of all those processes where the Vicsek model is relevant.…”

Neurophysiological control of swimming behaviour, attachment and metamorphosis in black-footed abalone (Haliotis iris) larvae

“…This reduction in swimming activity is interpreted as a decrease in ciliary movement caused by exposure to the treatments. While this is the first evidence of such an effect on larval behavior for this species, previous studies have investigated the neuronal control of larval ciliary movement in a number of mollusc species and considerable efforts have been made to characterize and map the neural circuit architectures involved (Jékely et al 2008). Results from these studies frequently reveal that patterns of cilia-based locomotion, velar ciliary beat frequency and the rate and duration of ciliary arrests are under dual innervation by excitory serotonergic and inhibitory dopaminergic mechanisms ( Croll & Dickinson 2004;Braubach et al 2006;Croll 2009).…”