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Abstract
BackgroundVisual perception is initiated in the photoreceptor cells of the retina via the phototransduction system. This system has shown marked evolution during mammalian divergence in such complex attributes as activation time and recovery time. We have performed a molecular evolutionary analysis of proteins involved in mammalian phototransduction in order to unravel how the action of natural selection has been distributed throughout the system to evolve such traits.ResultsWe found selective pressures to be non-randomly distributed according to both a simple protein classification scheme and a protein-interaction network representation of the signaling pathway. Proteins which are topologically central in the signaling pathway, such as the G proteins, as well as retinoid cycle chaperones and proteins involved in photoreceptor cell-type determination, were found to be more constrained in their evolution. Proteins peripheral to the pathway, such as ion channels and exchangers, as well as the retinoid cycle enzymes, have experienced a relaxation of selective pressures. Furthermore, signals of positive selection were detected in two genes: the short-wave (blue) opsin (OPN1SW) in hominids and the rod-specific Na+/ Ca2+, K+ ion exchanger (SLC24A1) in rodents.ConclusionsThe functions of the proteins involved in phototransduction and the topology of the interactions between them have imposed non-random constraints on their evolution. Thus, in shaping or conserving system-level phototransduction traits, natural selection has targeted the underlying proteins in a concerted manner.
Highlights
Visual perception is initiated in the photoreceptor cells of the retina via the phototransduction system
System-wide distribution of selective pressures In total, 57 genes were identified as being directly relevant to the phototransduction system in mammals, including genes encoding proteins of the signaling cascade, the retinoid cycle, and key proteins involved in the final steps of photoreceptor cell-type determination
We have provided evidence that, during the divergence of primates, natural selection has tuned the performance of the first steps of vision through non-random targeting of member proteins within the system
Summary
Visual perception is initiated in the photoreceptor cells of the retina via the phototransduction system. This system has shown marked evolution during mammalian divergence in such complex attributes as activation time and recovery time. The opsins trigger a prototypical G-protein-coupled receptor-mediated signaling cascade that amplifies the opsin response and results in the hyperpolarization of the cell. This initiates a neuronal signal that is transmitted to the visual cortex in the brain for processing. A well-known evolutionary development in mammalian phototransduction is in the evolution of the cone opsin repertoire. Primates have developed the fovea, a highly concentrated region composed exclusively of cone cells in the center of the retina, which imparts very high acuity
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