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, 30 (1-2), 5-20

Eye Evolution and Its Functional Basis

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Eye Evolution and Its Functional Basis

Dan-E Nilsson. Vis Neurosci.

Abstract

Eye evolution is driven by the evolution of visually guided behavior. Accumulation of gradually more demanding behaviors have continuously increased the performance requirements on the photoreceptor organs. Starting with nondirectional photoreception, I argue for an evolutionary sequence continuing with directional photoreception, low-resolution vision, and finally, high-resolution vision. Calculations of the physical requirements for these four sensory tasks show that they correlate with major innovations in eye evolution and thus work as a relevant classification for a functional analysis of eye evolution. Together with existing molecular and morphological data, the functional analysis suggests that urbilateria had a simple set of rhabdomeric and ciliary receptors used for directional photoreception, and that organ duplications, positional shifts and functional shifts account for the diverse patterns of eyes and photoreceptors seen in extant animals. The analysis also suggests that directional photoreception evolved independently at least twice before the last common ancestor of bilateria and proceeded several times independently to true vision in different bilaterian and cnidarian groups. This scenario is compatible with Pax-gene expression in eye development in the different animal groups. The whole process from the first opsin to high-resolution vision took about 170 million years and was largely completed by the onset of the Cambrian, about 530 million years ago. Evolution from shadow detectors to multiple directional photoreceptors has further led to secondary cases of eye evolution in bivalves, fan worms, and chitons.

Figures

Fig. 1.
Fig. 1.
The causality of different levels in the evolution of sensory systems. The genome, which is the level directly subject to heritable variation, generates the morphology and physiology, which in turn generates behavior guided by sensory information, and this in turn generates the fitness that selection can act upon. In this view, sensory-guided behavior is entirely a consequence of the morphology and physiology. From this, it follows that genetic modifications are driven by modified requirements on the morphology and physiology, which in turn are driven by modified requirements on sensory-guided behavior and finally by requirements for improved fitness. This is different to the view of Endler (1992), who considers sensory organs and behavior to coevolve, but the sensory organs are then seen in isolation from the rest of the morphology and physiology of the organism. The two views are not in logical conflict, but the view illustrated here gives a more important role to behaviors, as the causal evolutionary link between fitness and sensory systems (which are part of the organisms’ morphology/physiology).
Fig. 2.
Fig. 2.
Minimum intensities from Table 1, for the four classes of sensory tasks, plotted together with the daily variation of natural luminances and daylight intensities at different depths in clear water. Blue indicates calculations for a 10 µm diameter cell with no membrane stacking and no focusing optics (just screening to obtain the desired detection angle). Calculations for membrane stacking are indicated by green and for focusing optics (and membrane stacking) by red. The color gradients at the lower end of the bars show the range of gradually decreasing function between the primary values from Table 1 (dotted lines), and the bracketed values where sensory information is assumed too poor for the task.
Fig. 3.
Fig. 3.
Schematic illustration of the evolution of photoreceptive behaviors on a vertical scale of task complexity, with the position of major functional innovations indicated. The line for directional photoreception is dashed to indicate that class II tasks may become superfluous by the evolution of class III tasks, whereas the other classes remain relevant after a higher class has evolved. Eyes capable of class IV tasks can of course still handle class III tasks. The corresponding receptor/eye morphologies are shown to the right. Note that compound and single chambered eyes are principally different solutions suggesting independent transitions from class II to class III.
Fig. 4.
Fig. 4.
Semischematic drawings of receptor morphologies for class II photoreception (A, B) and eyes for class III or low-resolution vision (C, D). The single cell eyespots of cubozoan planula-larvae (A) are not neurons but assumed to function both as photoreceptor and effector organs through the motile cilium. The two-cell eyespot of a polychaete larva (B) contains a rhabdom-bearing receptor cell and a pigment cell. The typical flatworm version of a pigment-cup eye (C) is formed by one or a few pigments cells forming a cup around a number of rhabdom-bearing photoreceptor cells. The lens eye of a cubozoan jellyfish (D) is functionally closer to a flatworm cup-eye than it is to the camera eyes of vertebrates or cephalopods. The lens-like body filling the eyecup does at best place a focus just below the retina, but in some species, it barely has any focusing function at all (Nilsson et al., ; O’Connor et al., 2009). In the cubozoan eye, the receptors are of the ciliary type, and the screening pigment is contained in the receptor cells rather than in specialized pigment cells.
Fig. 5.
Fig. 5.
Eyes serving class IIb tasks (optical predator alarms). The reflector-cup eyes of scallop, Pecten maximus (A) and the lens-less compound eyes of ark clams (B) are found in large numbers on the mantle edge. In fan worms (Sabella melanostigma), pairs of eyes are found at regular intervals along the feeding tentacles (C). A section through the fan-worm eyes (D) reveals ommatidia shielded by pigment tubes, and lenses that improve both photon catch and directionality (Nilsson, 1994).
Fig. 6.
Fig. 6.
Possible evolutionary transitions between classes of photoreceptive sensory tasks and related sensory structures. For functional reasons, the process cannot skip classes except for reductions (dashed line) when functions are lost through behavioral modifications. The color coding agrees with Figs. 2, 6, and 7. Note that the classes concern only the spatial modality of photoreception, which is fundamental for eye evolution. The other photoreceptive modalities, color and polarization, are very important for the visual ecology of many species but not so much for the evolution of eye design. Class II organs are appropriately called eyespots because the screening pigment makes them visible, but they do not provide vision (image information) and are thus not true “eyes.”
Fig. 7.
Fig. 7.
The classes of photoreceptive tasks plotted on a metazoan phylogeny, using the arguments from the functional discussion in this paper together with information on receptor morphology (mainly from Salvini-Plawen & Mayr, 1977), and the occurrence of opsins (Plachetzki et al., ; Porter et al., ; Schnitzler et al., 2012). For clarity, minor bilaterian taxa were omitted, and because these only have class II photoreception, the most parsimonious transitions to class III are the ones indicated by color. The exact pattern of transitions should be interpreted with caution because it is sensitive to the choice of phylogenetic tree, which is here based on Philippe et al. (2009), with the placement of the Acoela according to Philippe et al. (2007).
Fig. 8.
Fig. 8.
Schematic view of the head region of bilateria indicating the evolutionary shift of position and function of photoreceptor organs argued for in the text. The photoreceptor/opsin types are denoted by (r) for rhabdomeric/r-opsin and (c) for ciliary/c-opsin. Note that the vertebrate lateral eyes are composite structures formed by fusion of components from different photoreceptor organs in Urbilateria. It is also possible that vertebrate ancestors went through a stage with only median eyes (Vopalensky et al., 2012). Polychaetes have only made functional shifts and duplicated their lateral rhabdomeric eyes, whereas crustaceans/insects have formed a new median eye from rhabdomeric photoreceptors.

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