Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments

Abstract

The squirrel monkey (Saimiri sciureus) exhibits a polymorphism of colour vision: some animals are dichromatic, some trichromatic, and within each of these classes there are subtypes that resemble the protan and deutan variants of human colour vision. For each of ten individual monkeys we have obtained (i) behavioural measurements of colour vision and (ii) microspectrophotometric measurements of retinal photopigments. The behavioural tests, carried out in Santa Barbara, included wavelength discrimination, Rayleigh matches, and increment sensitivity at 540 and 640 nm. The microspectrophotometric measurements were made in London, using samples of fresh retinal tissue and a modified Liebman microspectrophotometer: the absorbance spectra for single retinal cells were obtained by passing a monochromatic measuring beam through the outer segments of individual rods and cones. The two types of data, behavioural and microspectrophotometric, were obtained independently and were handed to a third party before being interchanged between experimenters. From all ten animals, a rod pigment was recorded with $\lambda _{\max}$ (wavelength of peak absorbance) close to 500 nm. In several animals, receptors were found that contained a short-wave pigment (mean $\lambda _{\max}$ = 433.5 nm): these violet-sensitive receptors were rare, as in man and other primate species. In the middle- to long-wave part of the spectrum, there appear to be at least three possible Saimiri photopigments (with $\lambda _{\max}$ values at about 537, 550 and 565 nm) and individual animals draw either one or two pigments from this set, giving dichromatic or trichromatic colour vision. Thus, those animals that behaviourally resembled human protanopes exhibited only one pigment in the red--green range, with $\lambda _{\max}$ = 537 nm; other behaviourally dichromatic animals had single pigments lying at longer wavelengths and these were the animals that behaviourally had higher sensitivity to long wavelengths. Four of the monkeys were behaviourally judged to be trichromatic. None of the latter animals exhibited the two widely separated pigments (close to 535 and 567 nm) that are found in the middle- and long-wave cones of macaque monkeys. But the spread of $\lambda _{\max}$ values for individual cones was greater in the trichromatic squirrel monkeys than in the dichromats; than in the case of three, behaviourally deuteranomalous, trichromats there was clear evidence that the distribution of $\lambda _{\max}$ values was bimodal, suggesting photopigments at approximately 552 and 565 nm. The fourth, behaviourally protanomalous, trichromat exhibited a spread of individual $\lambda _{\max}$ values that ranged between 530 and 550 nm. Good quantitative agreement was found when the microspectrophotometrically measured absorbance spectra were used to predict the behavioural sensitivity of individual animals to long wavelengths. The concordance of the two sets of measurements places beyond question the existence of a polymorphism of colour vision in Saimiri sciureus and suggests that the behavioural variation arises from variation in the retinal photopigments. Heterozygous advantage may explain the polymorphism.