Filter-Mediated Color Vision with One Visual Pigment

Kong, King-Leung; Fung, Yau Man; Wasserman, Gerald S.

doi:10.1126/science.7352289

Cited by 19 publications

(11 citation statements)

References 10 publications

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“…Detecting different colors has been achieved in most species through the evolution of retinal photoreceptors that are maximally sensitive to different wavelengths of light. In a few cases, however, filters positioned in front of photopigments offer another solution (see Kong, Fung, and Wasserman 1980;Ohtsuka 1985). The brain is informed about the detected chromatic differences via color-opponent neurons (see Daw 1967).…”

Section: Teleost Photoreceptorsmentioning

confidence: 99%

Aquatic Adaptations in Fish Eyes

Fernald

1988

Sensory Biology of Aquatic Animals

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To suppose that the eye with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts oflight, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest degree.(Charles Darwin, The Origin of Species, 1859, p. 168) Of all the sense organs, eyes have probably attracted the most attention because of both their central importance and intricate construction. Darwin knew that such "organs of extreme perfection and complication" posed a crucial test of his theory because they seemed too good to have been shaped by natural selection (Darwin [1859(Darwin [ ] 1958. Since eyes must obey the optical laws of physics, fundamental physical constraints on their structure provide an important analytical basis for understanding adaptive ocular specializations. In light of these physical constraints, inferences about the selective forces that have shaped eye design can be made with some confidence, particularly in the study of aquatic eyes.Fish eyes offer an unusually interesting and accessible opportunity to ask general questions about visual evolution, development, and function (Fernald 1984). Although a great deal of work has been done on the domestic goldfish, this narrow experimental focus obscures the fact that bony fish form the largest class of vertebrates, comprising over 25,000 species. Evidence of their success can be found in the adaptive radiation of forms occupying an extraordinary range of habitats. Fish eyes and brains variously reflect success in mastering different life history strategies with the unsurprising general rule that the favored sensory modality occupies disproportionately more brain volume (see Geiger 1956).There are several summaries of information about the fish eye available, so here I will present primarily recent findings. Since fish eyes have a relatively standard construction, with some deviations resulting from adaptations to specialized situations, I will first discuss underlying physical constraints that apply generally to the evolution of eyes. Then I will analyze various structures that have evolved to meet these constraints in teleost fish and, finally, present some new evidence about novel solutions to problems posed by regulation of fish eye growth.

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Section: Teleost Photoreceptorsmentioning

confidence: 99%

Aquatic Adaptations in Fish Eyes

Fernald

1988

Sensory Biology of Aquatic Animals

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“…The presence of molecules other than opsins in the receptor cells can filter the light traveling inside the rhabdom, modifying the spectral sensitivity of the receptor (Goldsmith and Bernard, 1974;Kong et al, 1980). In butterflies (with the exception of papilionids) a tapetum basal to the rhabdom reflects either broadband light (300-700·nm) as in Vanessa cardui (Briscoe et al, 2003), or relatively narrow-band light (320-590·nm)…”

Section: Introductionmentioning

confidence: 99%

“…In these cases, color discrimination could theoretically be extended by means of filtering pigments but direct behavioral evidence confirming this is missing. Different corneal filters in different ommatidia found in tabanid flies and grasshoppers have the same potential to create new receptor types (Kong et al, 1980;Lunau and Knüttel, 1995).…”

Section: Introductionmentioning

confidence: 99%

Color discrimination in the red range with only one long-wavelength sensitive opsin

Zaccardi

Kelber

Sison-Mangus

et al. 2006

Journal of Experimental Biology

107

147

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SUMMARY The basic precondition for color vision is the presence of at least two receptor types with different spectral sensitivities. The sensitivity of a receptor is mostly defined by the opsin-based visual pigment expressed in it. We show here, through behavioral experiments, that the nymphalid butterfly Heliconius erato, although it expresses short and medium wavelength opsins and only one long wavelength opsin, discriminates colors in the long-wavelength range (590 nm, 620 nm and 640 nm), whereas another nymphalid, Vanessa atalanta, despite having color vision, is unable to do so. In the eyes of H. erato we identified filtering pigments very close to the rhabdom which differ between ommatidia and produce the yellow and red ommatidial reflection seen under orthodromic illumination. The eyes of V. atalanta lack the filtering pigments, and reflect a homogeneous orange. We hypothesize that the filtering pigments found in the eyes of H. erato may shift the spectral sensitivity peak of the long wavelength receptors in some ommatidia towards longer wavelengths. The comparison of the signals between the two new receptor types makes color discrimination in the red range possible. To our knowledge, this is the first behavioral proof of color vision based on receptors expressing the same opsin.

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“…The trend for less-frequent strikes on prey by conspicuous males together with the higher rate of strikes that were successful by males painted inconspicuously support the hypothesis that conspicuous coloration reduces foraging efficiency through a reduction in aggressive crypsis. Because C. collaris is an ambush predator that primarily takes orthopterans capable of detecting wavelengths corresponding to the green body hues of males (Kong et al 1980;Wasserman and Kong 1982;Bailey and Harris 1991), green/yellow coloration may make lizards more visible to prey. The observation that males painted inconspicuously had a higher foraging success strongly suggests that brown coloration promoted their ability to remain inconspicuous until prey approached to within effective striking distance.…”

Section: Discussionmentioning

confidence: 99%

“…If increased predator attacks force conspicuously colored individuals to spend more time taking refuge (Martín and López 2001) which for AL collared lizards are abundant rock crevices , then the ability of lizards to scan for prey should be compromised, reducing their food intake. There is also considerable evidence that orthopterans (the major prey of collared lizards at AL) discriminate spectra ranging from 525 to 570 nm and respond strongly to wavelengths that appear green to humans (Kong et al 1980, Wasserman and Kong 1982, Bailey and Harris 1991. Green is the primary hue developed by 2y1 male collared lizards ) that spectral data have shown are the most conspicuous against the background at the AL site (Macedonia et al 2004).…”

mentioning

confidence: 99%

A growth cost of experimentally induced conspicuous coloration in first-year collared lizard males

Baird

2008

Behavioral Ecology

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I used painted first-year collared lizard males in the field to test the hypothesis that conspicuous coloration imposes a growth cost, either because it makes lizards less cryptic to their prey or because conspicuous color attracts predators forcing increased refuging by lizards. To make males more conspicuous, I painted them green and yellow to match hues of older territorial males, made another group inconspicuous by painting males brown like females, and painted a control group with water. I then compared rates of travel, the frequency, and the percentage of strikes on prey that were successful. I recaptured males periodically to record cloacal and substrate temperatures, to measure growth rate, and to retouch paint. Time spent refuging, travel rate, and both cloacal and substrate temperatures were similar in the 3 groups. Males painted conspicuously had slower growth than males in the other treatment groups. Inconspicuous males initiated strikes on prey more than 4 times more frequently than conspicuous males, and the number of strikes that resulted in prey capture was higher in inconspicuous males, suggesting that conspicuous coloration reduces foraging opportunities because it makes first-year males more visible to their prey. Rapid growth during the first season is necessary for collared lizard males to become large enough to compete for breeding territories as 2 year olds. Therefore, conspicuous coloration may develop gradually in first-year collared lizard males to maintain crypsis, which promotes food intake sufficient for rapid growth to large size that has important consequences for future reproductive success.

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Filter-Mediated Color Vision with One Visual Pigment

Cited by 19 publications

References 10 publications

Aquatic Adaptations in Fish Eyes

Aquatic Adaptations in Fish Eyes

Color discrimination in the red range with only one long-wavelength sensitive opsin

A growth cost of experimentally induced conspicuous coloration in first-year collared lizard males

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