SWEENEY, A.*; DES MARAIS, D.L.; BAN, A.; JOHNSEN, S.; Duke University; Duke University; Duke University; Duke University: Evolving Refractive Index: How Lens Protein Evolution Contributed to High-Resolution Squid Vision

A lens with a graded refractive index is necessary for high-resolution animal vision. This graded refractive index is produced by a concentration gradient of a few kinds of protein. Here, using a synthesis of protein biochemistry, molecular phylogenetics, structural biochemical modeling, molecular dynamics and optical modeling, we show how the radiation and electrostatic evolution of squid lens proteins have likely been major contributors to the evolution of a high-resolution lens in squid eyes. Lenses of the squid Loligo opalescens are built primarily of lens-specific proteins that resulted from the extensive genetic radiation of an ancestral liver enzyme. There are two major clades within this lens-specific radiation; one of them has extremely high average net charge, and has experienced strong positive selection in the Loligo lineage. These two clades differ in both their electrostatic properties and in other amino acid polymorphisms that may promote the folding and stability of proteins in the highly charged clade. The exterior of the lens, with a low refractive index and low protein concentration contains more highly charged proteins than the interior of the lens that has a high refractive index and high protein concentration. Molecular dynamics and optical scattering models using our lens protein electrostatics, concentration and distribution data show that the evolution of variable electrostatic properties in lens proteins likely promotes the transparency and stability of Loligo�s high-resolution lens.