‘Distributed’ vision and the architecture of animal visual systems

ABSTRACT

More than a century of research, of which JEB has published a substantial selection, has highlighted the rich diversity of animal eyes. From these studies have emerged numerous examples of visual systems that depart from our own familiar blueprint, a single pair of lateral cephalic eyes. It is now clear that such departures are common, widespread and highly diverse, reflecting a variety of different eye types, visual abilities and architectures. Many of these examples have been described as ‘distributed’ visual systems, but this includes several fundamentally different systems. Here, I re-examine this term, suggest a new framework within which to evaluate visual system distribution in both spatial and functional senses, and propose a roadmap for future work. The various architectures covered by this term reflect three broad strategies that offer different opportunities and require different approaches for study: the duplication of functionally identical eyes, the expression of multiple, functionally distinct eye types in parallel and the use of dispersed photoreceptors to mediate visual behaviour without eyes. Within this context, I explore some of the possible implications of visual system architecture for how visual information is collected and integrated, which has remained conceptually challenging in systems with a large degree of spatial and/or functional distribution. I highlight two areas that should be prioritised in future investigations: the whole-organism approach to behaviour and signal integration, and the evolution of visual system architecture across Metazoa. Recent advances have been made in both areas, through well-designed ethological experiments and the deployment of molecular tools.