Spectral discrimination in color blind animals via chromatic aberration and pupil shape
Alexander L. Stubbs a,b,1,2 and Christopher W. Stubbs c,d,2
aMuseum of Vertebrate Zoology, University of California, Berkeley, CA 94720;
bDepartment of Integrative Biology, University of California, Berkeley, CA 94720;
cDepartment of Physics, Harvard University, Cambridge, MA 02138;
dDepartment of Astronomy, Harvard University, Cambridge, MA 02138
Edited by John Mollon, University of Cambridge, Cambridge, United Kingdom, and accepted by Editorial Board Member Jeremy Nathans May 23, 2016 (received for review December 13, 2015)
We describe a means of obtaining spectral information using the principles of physical optics and an off-axis pupil shape without requiring spectrally distinct photoreceptor classes. The mechanism described here offers a possible solution to a long-standing puzzle in marine animals: cephalopods dramatically change color for both producing chromatically matched camouflage and signaling to conspecifics, despite having a single photoreceptor channel. The ability of these animals to achieve such excellent color matching to their surroundings, despite being “color blind” in the traditional sense, can be understood if they exploit chromatic aberration to deduce spectral information. The bizarre off-axis pupils of these animals can be understood as an adaptation that maximizes spectral information, even at the expense of image acuity.
We present a mechanism by which organisms with only a single photoreceptor, which have a monochromatic view of the world, can achieve color discrimination. An off-axis pupil and the principle of chromatic aberration (where different wavelengths come to focus at different distances behind a lens) can combine to provide “color-blind” animals with a way to distinguish colors. As a specific example, we constructed a computer model of the visual system of cephalopods (octopus, squid, and cuttlefish) that have a single unfiltered photoreceptor type. We compute a quantitative image quality budget for this visual system and show how chromatic blurring dominates the visual acuity in these animals in shallow water. We quantitatively show, through numerical simulations, how chromatic aberration can be exploited to obtain spectral information, especially through nonaxial pupils that are characteristic of coleoid cephalopods. We have also assessed the inherent ambiguity between range and color that is a consequence of the chromatic variation of best focus with wavelength. This proposed mechanism is consistent with the extensive suite of visual/behavioral and physiological data that has been obtained from cephalopod studies and offers a possible solution to the apparent paradox of vivid chromatic behaviors in color blind animals. Moreover, this proposed mechanism has potential applicability in organisms with limited photoreceptor complements, such as spiders and dolphins.
spectral discrimination chromatic aberration color vision pupil shape cephalopod
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