How the vertebrate eye, as we know it, has emerged over evolutionary time

The evolution of complex and physiologically remarkable structures such as the vertebrate eye has long been a focus of intrigue and theorizing by biologists.

In work reported in Current Biology, the evolutionary history of a critical eye protein has revealed a previously unrecognized relationship between certain components of vertebrate eyes and those of the more primitive light-sensing systems of invertebrates.

The findings help clarify our conceptual framework for understanding how the vertebrate eye, as we know it, has emerged over evolutionary time.

The work is reported by Sebastian Shimeld at the University of Oxford and colleagues at the University of London and Radboud University in The Netherlands.

Our sight relies on the ability of our eye to form a clear, focused image on the retina. The critical component in focusing is the eye lens, and the physical properties that underlie the transparency of the lens, as well as its ability to precisely refract light, arise from the high concentrations of special proteins called crystallins found in lens cells.

Fish, frogs, birds and mammals all experience image-forming vision, thanks to the fact that their eyes all express crystallins and form a lens; however, the vertebrates' nearest invertebrate relatives, such as sea squirts, have only simple eyes that detect light but are incapable of forming an image. This has lead to the view that the lens evolved within the vertebrates early in vertebrate evolution, and it raises a long-standing question in evolutionary biology: How could a complex organ with such special physical properties have evolved?

In their new work, Shimeld and colleagues approached this question by examining the evolutionary origin of one crystallin protein family, known as the ß?-crystallins. Focusing on sea squirts, invertebrate cousins of the vertebrate lineage, the researchers found that these creatures possess a single crystallin gene, which is expressed in its primitive light-sensing system. The identification of the sea squirt's crystallin strongly suggests that it is the single gene from which the vertebrate ß?-crystallins evolved.

The researchers also found that, remarkably, expression of the sea squirt crystallin gene is controlled by genetic elements that also respond to the factors that control lens development in vertebrates: The researchers showed that when regulatory regions of the sea squirt gene are transferred to frog embryos, these regulatory elements drive gene expression in the tadpoles' own visual system, including the lens. This strongly suggests that prior to the evolution of the lens, there was a regulatory link between two tiers of genes: those that would later become responsible for controlling lens development, and those that would help give the lens its special physical properties. This combination of genes appears to have then been co-opted in an early vertebrate during the evolution of its visual system, giving rise to the lens.