Elephants and Human Color-Blind Deuteranopes Have Identical Sets of Visual Pigments
Shozo Yokoyama*,1, Naomi Takenaka*, Dalen W. Agnew
and Jeheskel Shoshani
,
* Department of Biology, Emory University, Atlanta, Georgia 30322
Department of Pathology, Microbiology and Immunology, University of California, Davis, California 95616
Department of Biology, University of Asmara, Asmara, Eritrea
Elephant Research Foundation, Bloomfield Hills, Michigan 48304
1Corresponding author: Department of Biology, Rollins Research Center, Emory University, 1510 Clifton Rd., Atlanta, GA 30322.
Being the largest land mammals, elephants have very few natural enemies and are active during both day and night. Compared with those of diurnal and nocturnal animals, the eyes of elephants and other arrhythmic species, such as many ungulates and large carnivores, must function in both the bright light of day and dim light of night. Despite their fundamental importance, the roles of photosensitive molecules, visual pigments, in arrhythmic vision are not well understood. Here we report that elephants (Loxodonta africana and Elephas maximus) use RH1, SWS1, and LWS pigments, which are maximally sensitive to 496, 419, and 552 nm, respectively. These light sensitivities are virtually identical to those of certain "color-blind" people who lack MWS pigments, which are maximally sensitive to 530 nm. During the day, therefore, elephants seem to have the dichromatic color vision of deuteranopes. During the night, however, they are likely to use RH1 and SWS1 pigments and detect light at 420–490 nm.
Genetics, Vol. 170, 335-344, May 2005
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VERTEBRATES can be classified roughly into diurnal, nocturnal, and arrhythmic species according to their visual habits. The eyes of diurnal animals contain predominantly cone photoreceptor cells and are specifically designed for high visual acuity during the day, whereas those of nocturnal animals contain predominantly rod cells and are designed to operate mostly under low illuminations at night (WALLS 1942; ALI and KLYNE 1985). Compared to these, the eyes of the arrhythmic, known also as cathemeral, species seem to function equally in bright light hours of day and dim ones of night (NOWAK 1991). The large terrestrial mammals such as ungulates, elephants, and large carnivores have arrhythmic vision (WALLS 1942; ALI and KLYNE 1985). These animals typically contain abundant populations of rods in their retinas, which are often found in conjunction with a retinal tapetum (JACOBS et al. 1994). To react to changes in light intensities relatively quickly, many arrhythmic species not only elongate the rods and contract the cones in light and execute the opposite movements in darkness but also regulate the amount of light reaching the retina by changing the size of the pupil (WALLS 1942; ALI and KLYNE 1985).
Despite their fundamental importance in vision, the role of visual pigments in arrhythmic vision is not well understood. Visual pigments consist of a transmembrane (TM) protein, an opsin, and the 11-cis-retinal chromophore. They are classified into rhodopsins (RH1), RH1-like (RH2), short wavelength-sensitive type 1 (SWS1), short wavelength-sensitive type 2 (SWS2), and middle and long wavelength-sensitive (M/LWS) pigment groups (YOKOYAMA and YOKOYAMA 1996; YOKOYAMA 2000a; EBREY and KOUTALOS 2001). The RH2 and SWS2 opsin genes became nonfunctional in the early stage of mammalian evolution (YOKOYAMA and YOKOYAMA 1996) and the RH1, SWS1, and M/LWS pigments in the mammalian ancestor had the wavelengths of maximal absorption (
max) of 
500, 360, and 560 nm, respectively (YOKOYAMA 2000a; YOKOYAMA and RADLWIMMER 2001; EBREY and TAKAHASHI 2002; SHI and YOKOYAMA 2003). The respective groups of visual pigments in arrhythmic mammals have max-values of 497–508, 428–456, and 531–555 nm (Table 1). In the arrhythmic mammals, therefore, the max-values of RH1 pigments have been maintained more or less at the ancestral level, but those of SWS1 pigments have increased significantly and those of M/LWS pigments have decreased.
Elephants can be trained to paint and their paintings have been sold in auction (GILBERT 1990; TENNESEN 1998). This "artistic ability" suggests a reasonably well-developed color vision of elephants. Thus, it is of interest to study what types of visual pigments elephants possess and how they compare to those of other arrhythmic animals. To explore the possible roles of visual pigments in the arrythmic vision of mammals, we have cloned the opsin genes from African elephant (Loxodonta africana) and Asian elephant (Elephas maximus), which are evolutionarily distantly related to the arrhythmic mammals studied to date (EIZIRIK et al. 2001). The results show that the elephants use RH1, SWS1, and LWS pigments, which have max-values of 496, 419, and 552 nm, respectively. These spectral sensitivities are virtually identical to those of certain human deuteranopes who lack MWS pigments. Therefore, elephants seem to have the dichromatic color vision of these deuteranopes. The mutagenesis results show that the max-values of the elephant RH1, SWS1, and LWS pigments have been attained by D83N, F86S/T93I/L116V, and S180A, respectively.
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