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.

Visual navigation in starfish: first evidence for the use of vision and eyes in starfish

“…Our data also shed light on another aspect of eye evolution. It has been proposed that major steps in eye evolution, such as implementation of spatial resolution and true optics, have been tightly connected to the acquisition of new visually guided behaviours [30]. It is suggested that early in eye evolution, animals possessed few and simple visually guided behaviours, requiring only simple eyes and simple nervous systems.…”

Spotlight on the evolution of vision

“…Colley and Dowling 2 pressures on visually guided behavior that favored one path at the expense of another (Nilsson & Arendt, 2008 ;Nilsson, 2009 ).…”

“…A sequence of stages has been envisioned to explain how a primitive eyespot evolved to become a complex camera-type eye (Nilsson & Arendt, 2008 ;Nilsson, 2009 ). In multicellular organisms, these fl at eyespots can be simple single-cell photoreceptors, scattered on the surface.…”

“…However, in order to further increase visual acuity, the aperture would need to be so small that it would shut out much light. So a lens was needed, and, subsequently, the image became sharper and sharper as eye evolution proceeded to produce the complex camera-type human eye (Nilsson & Arendt, 2008 ;Nilsson, 2009 ). Despite the perceived simplicity of microbes, jellyfi sh, worms, fruit fl ies and fi sh, they are remarkably complex creatures with genetic make-ups that are surprisingly similar to our own.…”

“…In studying evolution, it is often found that molecular data point in one direction and morphological fi ndings in another (Nilsson & Arendt, 2008 ;Nilsson, 2009 ). First, Nilsson provides new details on how eye evolution is directed by the demands of visually guided behavior.…”