Elephants and human color-blind deuteranopes have identical sets of visual pigments

Abstract

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.

Figure 1.—

Oligonucleotide primers for RT-PCR amplification and 5′- and 3′-RACE of RH1, SWS1, and M/LWS opsin mRNAs. (A) All internal primers are expected to amplify the codon positions between 248 and 300 of all opsin cDNAs and the RH1-, SWS1-, and LWS-specific internal primers are expected to amplify the codon positions between 50–70 and 260–280. (B) The EcoRI and SalI sites are boxed in the forward and reverse primers, respectively, and were used for cloning the amplified products into the expression vector pMT5. A Kozak sequence (CCACC) was inserted between the EcoRI site and the initiation codon to promote translation.

Figure 2.—

The dark absorption spectra of the elephant RH1, SWS1, and LWS pigments. The dark-light difference spectra are shown in the insets.

Figure 3.—

The phylogenetic tree of some representative RH1, SWS1, and LWS pigments. The numbers after P and at the nodes refer to λ_max-values. Zebrafish (Danio rerio), cavefish (Astyanax fasciatus), goldfish (Carassius auratus), coelacanth (Latimeria chalamnae), frog (Xenopus laevis), salamander (Ambystoma tigrinum), pigeon (Columba livia), zebra finch (Taeniopygia guttata), chameleon (Anolis carolinensis), human (Homo sapiens), bovine (Bos taurus), dolphin (Tursiops truncates), mouse (Mus musculus), and elephant (Loxodonta africana) are shown. The λ_max-values of the ancestral SWS1 and M/LWS pigments are taken from Shi and Yokoyama (2003) and Yokoyama and Radlwimmer (2001), respectively. Amino acid changes whose λ_max-shifts are not evaluated are shown in parentheses. The branch lengths are not to scale.