What has driven the evolution of multiple cone classes in visual systems: object contrast enhancement or light flicker elimination?

Sabbah and Hawryshyn BMC Biology 2013, 11:77 http://www.biomedcentral.com/1741-7007/11/77 RESEARCH ARTICLE Open Access What has driven the evolution of multiple cone classes in visual systems: object contrast enhancement or light flicker elimination? Shai Sabbah1* and Craig W Hawryshyn1,2 Abstract Background: Two competing theories have been advanced to explain the evolution of multiple cone classes in vertebrate eyes. These two theories have important, but different, implications for our understanding of the design and tuning of vertebrate visual systems. The ‘contrast theory’ proposes that multiple cone classes evolved in shallow-water fish to maximize the visual contrast of objects against diverse backgrounds. The competing ‘flicker theory’ states that multiple cone classes evolved to eliminate the light flicker inherent in shallow-water environments through antagonistic neural interactions, thereby enhancing object detection. However, the selective pressures that have driven the evolution of multiple cone classes remain largely obscure. Results: We show that two critical assumptions of the flicker theory are violated. We found that the amplitude and temporal frequency of flicker vary over the visible spectrum, precluding its cancellation by simple antagonistic interactions between the output signals of cones. Moreover, we found that the temporal frequency of flicker matches the frequency where sensitivity is maximal in a wide range of fish taxa, suggesting that the flicker may actually enhance the detection of objects. Finally, using modeling of the chromatic contrast between fish pattern and background under flickering illumination, we found that the spectral sensitivity of cones in a cichlid focal species is optimally tuned to maximize the visual contrast between fish pattern and background, instead of to produce a flicker-free visual signal. Conclusions: The violation of its two critical assumptions substantially undermines support for the flicker theory as originally formulated. While this alone does not support the contrast theory, comparison of the contrast and flicker theories revealed that the visual system of our focal species was tuned as predicted by the contrast theory rather than by the flicker theory (or by some combination of the two). Thus, these findings challenge key assumptions of the flicker theory, leaving the contrast theory as the most parsimonious and tenable account of the evolution of multiple cone classes. Keywords: Contrast hypothesis, Cone photoreceptors, Critical fusion frequency, Temporal contrast sensitivity, Opponent mechanisms, Color vision, Retina, Fish Background Multiple spectral classes of cones are found in the visual system of many vertebrates [1]. Comparison of the outputs of different cone classes enables color vision. Multiple cone classes appeared very early in vertebrate evolution, at least 540 MYA (million years ago) and perhaps as early as 700 MYA, prior to the separation of the jawed (Gnathostomata) and jawless (Agnatha) vertebrate lineages (approximately 485 MYA) [2,3]. This is based on the * Correspondence: 1 Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada Full list of author information is available at the end of the article presence of five classes of cone-like photoreceptors in the jawless Southern Hemisphere lamprey, Geotria australis [4-6], and three cone classes in the jawed cartilaginous fishes (Chondrichthyes) [7-9]. Additionally, cone opsins have been suggested to evolve prior to rod opsins [10], indicating that photopic (bright light) vision preceded scotopic (dim light) vision, and suggesting that these early vertebrates occupied brightly-lit shallow-water environments [11]. However, although the evolution of visual pigments has been studied extensively [1,4,6,10,12-20], the selective pressures that have driven the evolution of multiple cone classes in the eyes of vertebrates remain largely obscure. © 2013 Sabbah and Hawryshyn; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Sabbah and Hawryshyn BMC Biology 2013, 11:77 http://www.biomedcentral.com/1741-7007/11/77 Two competing theories have been advanced to explain the evolution of multiple cone classes; both assumed that vision in ancestral vertebrates utilized multiple cone photoreceptor classes, with color vision evolving only later as a byproduct. The ‘contrast theory’ of Munz and McFarland and McFarland and Munz [13,14] proposed that multiple cone classes evolved in shallow-water fish to maximize the visual contrast between objects and their background. Indeed, a single visual pigment (either rod or cone) may suffice to maximize the visual contrast between a given object and background. However, the need to maximize contrast between diverse objects and backgrounds of varying brightness and spectral characteristics was suggested to favor the appearance of multiple cone classes. The competing ‘flicker theory’ presented by Maximov [21] proposed that multiple cone classes have evolved to allow elimination of the flicker (fluctuation in light intensity) produced by variation in the refraction of sunlight at the water surface [22-25]. It was argued that subtraction of the output of one cone class from another through antagonistic (opponent) neural interactions would filter out the light flicker, yielding a flicker-free representation of the visual scene and enhancing object detection. The flicker theory has received relatively little attention; however, it has remained a competitor of the contrast theory, leaving the forces that have driven the evolution of multiple cone classes an open question. Both the contrast and flicker theories assume the presence of at least two cone classes that differ in spectral tuning. The flicker theory rests on three additional assumptions, one of which is the presence of antagonistic interactions between the output signals of the available cone classes. This assumption receives support from the presence of color-opponent horizontal cells [26,27] and the concentrically-antagonistic center-surround organization in retinal bipolar [28,29] and ganglion cells [30] in lower vertebrates. At least some of these color opponent mechanisms were probably present in early vertebrates that are represented today by the jawless lampreys [31-33]. However, two other critical assumptions of the flicker theory have so far not been seriously examined. First, it is assumed that ‘the [light] fluctuations are colorless, that is, the intensity of light changes synchronously in different parts of the spectrum’ [21]. Consequently, despite the strong fluctuations in light over the entire spectrum, the ratio of light intensities in two different parts of a spectru (...truncated)