The evolution of eyes and visually guided behaviour

Abstract

The morphology and molecular mechanisms of animal photoreceptor cells and eyes reveal a complex pattern of duplications and co-option of genetic modules, leading to a number of different light-sensitive systems that share many components, in which clear-cut homologies are rare. On the basis of molecular and morphological findings, I discuss the functional requirements for vision and how these have constrained the evolution of eyes. The fact that natural selection on eyes acts through the consequences of visually guided behaviour leads to a concept of task-punctuated evolution, where sensory systems evolve by a sequential acquisition of sensory tasks. I identify four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding, and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.

Figure 1.

Semi-schematic drawings of ocelli and simple eyes: (a) single cell ocellus of box jellyfish larva; (b) polychaete larval ocellus; (c) ocellus of acoel flatworm, with reflecting platelets in the pigment cell, but no membrane stacking in the two receptor cells; (d) inverse cup eye of planarian flatworm and (e) everse lens eye of juvenile box jellyfish. Photoreceptor cells are indicated by green shading. pr, screening pigment in receptor cell; mc, motile cilium; pc, specialized pigment cell; rh, rhabdom; r, reflective crystals; rc, receptive cilium.

Figure 2.

The four processes (a, molecular components; b, cell structures; c, cell types; d, organ shape) involved in eye evolution. The processes overlap in time, but are initiated in the ascending order.

Figure 3.

Hypothetical evolution of opsin function. For the underlying arguments, see text. The phylogenetic tree is according to Plachetzki et al. (2007).

Figure 4.

Natural luminances and the sensitivity of eyes. (a) Part of the diel light cycle, plotted on a log intensity scale. The range of luminances within a scene is constant, but slides up and down the log scale between day and night. Under overcast conditions, the whole luminance function is shifted down by up to 1 log unit. (b) The operational range of photoreceptors was modelled for non-directional monitoring of ambient luminance, directional scanning phototaxis and spatial vision (for calculations and data, see electronic supplementary material). Light green indicates the operational range for a photoreceptor without membrane extensions, and dark green is for the corresponding photoreceptor with a realistic amount of membrane stacking. The non-directional photoreceptor works to below starlight levels without any membrane stacking, but imaging eyes cannot discriminate luminances within a scene even in bright sunlight unless the photoreceptor membrane is extensively stacked. By combining large lenses, moderate resolution and slow vision, nocturnal and deep-sea animals can use their eyes at lower luminances than indicated by the rightmost green bar (Warrant 1999). (c) The depth in clear ocean water is plotted on the same luminance scale, assuming sunlight at the surface.

Figure 5.

Key innovations in eye evolution. Directional photoreception is assumed to have evolved from non-directional monitoring of ambient luminance by a cell duplication event and an opsin gene duplication leading to a receptor opsin and photoisomerase pair of proteins for efficient chromophore regeneration. This was followed by the introduction of screening pigment and soon also by membrane stacking to allow for better contrast discrimination, increased speed and more directional photoreception. Multiple receptor cells would then allow for true spatial vision and the scanning mode of operation could be abandoned. The single-chambered and compound eyes would have to evolve independently from directional ocelli. To collect enough photons for spatial vision with higher resolution, lenses must be introduced, but the new high-resolution tasks are expected to add to rather than replace the older low-resolution tasks.