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Review
, 371 (1685), 20150042

Phototaxis and the Origin of Visual Eyes

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Review

Phototaxis and the Origin of Visual Eyes

Nadine Randel et al. Philos Trans R Soc Lond B Biol Sci.

Abstract

Vision allows animals to detect spatial differences in environmental light levels. High-resolution image-forming eyes evolved from low-resolution eyes via increases in photoreceptor cell number, improvements in optics and changes in the neural circuits that process spatially resolved photoreceptor input. However, the evolutionary origins of the first low-resolution visual systems have been unclear. We propose that the lowest resolving (two-pixel) visual systems could initially have functioned in visual phototaxis. During visual phototaxis, such elementary visual systems compare light on either side of the body to regulate phototactic turns. Another, even simpler and non-visual strategy is characteristic of helical phototaxis, mediated by sensory-motor eyespots. The recent mapping of the complete neural circuitry (connectome) of an elementary visual system in the larva of the annelid Platynereis dumerilii sheds new light on the possible paths from non-visual to visual phototaxis and to image-forming vision. We outline an evolutionary scenario focusing on the neuronal circuitry to account for these transitions. We also present a comprehensive review of the structure of phototactic eyes in invertebrate larvae and assign them to the non-visual and visual categories. We propose that non-visual systems may have preceded visual phototactic systems in evolution that in turn may have repeatedly served as intermediates during the evolution of image-forming eyes.

Keywords: connectome; eye evolution; marine ciliated larva; opsin; photoreceptor; vision.

Figures

Figure 1.
Figure 1.
Diversity of simple eyes in planktonic larvae. Schematic drawings of simple eyes from marine invertebrate larvae. Rhabdomeric photoreceptors are shown in yellow, ciliary photoreceptors in blue, lenses in grey and pigment granules in black.
Figure 2.
Figure 2.
Transition scenario for the evolution of low-resolution visual eyes from two-celled sensory-motor eyes. (a) Larval eyespot with a single photoreceptor cell (orange) mediates positive helical phototaxis by directly innervating an effector (muscle and ciliated cells are not distinguished for simplicity). (b) A duplication event leads to the development of a second photoreceptor cell (blue), which is able to mediate negative phototaxis. The development of mutual synaptic contacts between the contralateral photoreceptors allows contrast enhancement, representing the first step towards vision. (c) Relocation and duplication of the second photoreceptor cell (blue) results in the development of the cerebral eyes. The duplication of photoreceptors improves the signal-to-noise ratio, the development of a lens improves photon collection. (d) Integration of a motor neuron into the circuit and bilateral circuit divergence enables the signal to reach either the left or the right motor organ (effector). With this circuit, the animal is able to switch between positive and negative phototaxis, using the same eye. (e,f) Integration of one to several interneurons improves computational power and provides further possibilities for modulation (e.g. integration of other sensory inputs). (g) The development of a new type of primary interneuron (magenta, directly postsynaptic to the photoreceptor cells), which transmits the signal with a delay. This second primary interneuron might work together with the first primary interneuron (yellow) to form the first motion detector. (h) The Reichardt detector, a conceptual model for motion detection, adapted from Haag et al. [105]. Orange, sensory–motor photoreceptor of the eyespot and motor neurons; blue, adult eye photoreceptors; yellow, primary interneuron; pink, green, magenta, other interneurons.

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