Visual Neuroscience

Evolution and eye design

Understanding the dermal light sense in the context of integrative photoreceptor cell biology

M. DESMOND RAMIREZa1, DANIEL I. SPEISERa1, M. SABRINA PANKEYa1 and TODD H. OAKLEYa1 c1

a1 Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California

Abstract

While the concept of a dermal light sense has existed for over a century, little progress has been made in our understanding of the mechanisms underlying dispersed photoreception and the evolutionary histories of dispersed photoreceptor cells. These cells historically have been difficult to locate and positively identify, but modern molecular techniques, integrated with existing behavioral, morphological, and physiological data, will make cell identification easier and allow us to address questions of mechanism and evolution. With this in mind, we propose a new classification scheme for all photoreceptor cell types based on two axes, cell distribution (aggregated vs. dispersed) and position within neural networks (first order vs. high order). All photoreceptor cells fall within one of four quadrants created by these axes: aggregated/high order, dispersed/high order, aggregated/first order, or dispersed/first order. This new method of organization will help researchers make objective comparisons between different photoreceptor cell types. Using integrative data from four major phyla (Mollusca, Cnidaria, Echinodermata, and Arthropoda), we also provide evidence for three hypotheses for dispersed photoreceptor cell function and evolution. First, aside from echinoderms, we find that animals often use dispersed photoreceptor cells for tasks that do not require spatial vision. Second, although there are both echinoderm and arthropod exceptions, we find that dispersed photoreceptor cells generally lack morphological specializations that either enhance light gathering or aid in the collection of directional information about light. Third, we find that dispersed photoreceptor cells have evolved a number of times in Metazoa and that most dispersed photoreceptor cells have likely evolved through the co-option of existing phototransduction cascades. Our new classification scheme, combined with modern investigative techniques, will help us address these hypotheses in great detail and generate new hypothesis regarding the function and evolution of dispersed photoreceptor cells.

(Received February 21 2011)

(Accepted April 13 2011)

(Online publication July 08 2011)

Correspondence:

c1 Address correspondence and reprint requests to: Todd H. Oakley, Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106. E-mail: oakley@lifesci.ucsb.edu