Visionary research: scientists delve into the evolution of color vision in primates.

The next time you appreciate the beauty of a rainbow or the subtle hues of an impressionist masterpiece, you'll be taking advantage of the human brain's palette of an estimated 2.3 million colors. Why do people and many nonhuman primate species have the capability to distinguish so many hues? How did it benefit our ancestors to evolve this trait? After all, most mammals seem to do just fine with a less-discerning color vision. Dogs, cats, and many other familiar mammals, for example, can't discriminate between reds and greens.

Perhaps the first person to address this issue was 19th-century biologist Grant Allen. His theory, developed while he was a professor in Jamaica, was that primates need their superior color vision to find fruits hidden among green leaves. The dazzling red, orange, and crimson colors of tropical fruits inspired his hypothesis, which he put forth in an 1879 book, The Colour Sense: Its Origin and Development.

Allen's book contained many flaws--he didn't realize that lemurs, which are primates in Madagascar, have the more limited form of mammalian color vision, for example--but his theory left its imprint. "His reasoning was faulty, but nevertheless it was such an intuitive idea that it's been reiterated ever since" says Nathaniel Dominy of Yale University.

In a new wrinkle on this evolutionary mystery, Dominy and Peter Lucas of the University of Hong Kong have recently challenged the dogma that trichromacy--the scientific name for the form of color vision people have--evolved for detecting ripe fruits. They argue that this color vision instead helped our primate ancestors find tender red leaves bursting with nutritional value.

Furthermore, other scientists have found some surprising possible consequences of the evolution of trichromacy. Several research teams have recently reported genetic evidence that human ancestors' sense of smell began to deteriorate at about the same time that they developed trichromacy. Indeed, that visual upgrade may explain why people and Old World primates have lost much of their response to pheromones, the odorless, airborne chemicals that drive the reproductive behaviors of many mammals.

"Maybe there's a trade-off," speculates Dominy. "As your visual system improves, maybe your olfactory system declines."

All this recent research, notes Daniel Osorio of University of Sussex in Brighton, England, "makes us ask, 'What do we see color for?'"

SEEING RED All vertebrates, from fish to people, see colors by using cells in the eyes called cones. Within the cones are light-sensitive pigments known as opsins. The pigments in different cones can vary in the wavelength of light to which they respond. An animal's brain distinguishes among colors by comparing the signals it receives from cones containing different opsins.

Take birds. Most have opsins sensitive to ultraviolet, blue, green, and red light, enabling them to recognize an unusually large range of wavelengths. In contrast, most mammals have just two opsins, one sensitive to blue and the other one to green. This form of color vision is known as dichromacy.

From this bird-mammal distinction, scientists have concluded that the evolutionary ancestor common to both had four distinct opsins. Early mammals then lost two of them, probably with little ill effect because these creatures were nocturnal and had a limited need to discern colors.

When it comes to their color vision, people fall between birds and most mammals. People generally have three opsins, which are sensitive to blue, green, and red. In fact, most of the primates that evolved in Africa and Asia, including the great apes and chimpanzees, are fully trichromatic. In contrast, most New World primates, such as the tamarins and marmosets of South America, are dichromatic, having just blue-sensitive and green-sensitive opsins.

People and birds don't have the same gene for their red-sensitive opsin. The primate version apparently arose anew in Old World primates from a duplication of the green opsin gene on the X chromosome 30 million to 40 million years ago, long after Africa and South America separated.

Over time, the extra gene accumulated mutations that made the protein it encodes sensitive to red instead of green light. By comparing the signals sent by cones containing red or green opsin, Old World primates could now make fine distinctions among reds, yellows, and greens. This newfound power must have given them a competitive advantage. The red and green opsin genes persist in all Old World primates alive today.

New World primates' vision changed, too, but not to full trichromacy. In most of these animals, some of the females discern reds and yellows from greens, but males don't. That's because the opsin gene on the X chromosome comes in several forms, each one encoding a pigment sensitive to a slightly different color in the red-green spectrum. Since females have two X chromosomes, they sometimes inherit two forms of the opsin gene that are different enough to give these females trichromacy. Males, with their single X chromosome, have just one version of this opsin gene, making all of them dichromatic.

Researchers are taking advantage of this unusual situation to look for benefits of color vision. They're examining New World-primate species in which animals can be either dichromatic or trichromatic. Several years ago, for example, Nancy G. Caine of California State University in San Marcos and Nick I. Mundy of the University of Oxford in England tested the capacity of marmosets from Brazil to find green- and orange-colored cereal balls scattered on green shavings of pine. Trichromatic female marmosets found the orange-colored balls more easily than males and dichromatic females did, but the groups were the same when it came to the green balls.

More recently, Mundy joined with Andrew C. Smith of the University of Stirling in Scotland and several other investigators for an even more realistic test of trichromacy's use. The researchers placed tamarins in an artificial environment mimicking the monkeys' natural one. Among green-paper leaves were boxes colored to correspond to ripe, ripening, or unripe versions of one of the tamarin's favorite fruits. The "riper" the box, the more fudge it contained, mirroring the increased desirability of ripe fruit.

Compared with their dichromatic relatives, trichromatic tamarins were both faster at finding the boxes among the artificial leaves and more efficient at picking the "ripe" ones, Smith, Mundy, and their colleagues report in Sept. 15 Journal of Experimental Biology. "The main finding is that trichromacy confers an advantage when selecting ripe fruits from those at various stages of maturity.... This is the first time such an advantage has been demonstrated for primates using naturalistic stimuli," the researchers assert.

FOOD FIGHT Dominy doesn't reject the notion that trichromacy can help primates find some fruits that ripen to a reddish or yellow hue. He does question whether that's benefit enough to have made trichromacy essential to Old World primates. Some of them eat little fruit, and some favorite fruits of the primates are black or green when ripe, he notes. Moreover, there may be better ways than reading color to establish whether a fruit is ripe. Some of Dominy's unpublished work suggests that primates use their sense of touch and smell to detect ripeness, for example.

The major challenge to the hypothesis that trichromacy evolved for finding fruit emerged in 1996, when Gerald H. Jacobs of the University of California, Santa Barbara and his colleagues reported that both male and female howler monkeys--New World primates that eat primarily leaves--have fully trichromatic vision. The monkeys all have a second opsin gene on their X chromosome. An ancestor of the howler monkeys had apparently matched the gene duplication that Old World monkeys experienced, yet the evolutionary force preserving the new opsin doesn't appear to have been an advantage in gathering fruit.

"It was a huge discovery that howler monkeys had independently evolved the same kind of color vision that monkeys from Africa and Southeast Asia had," says Dominy. "Why would the only monkey in South America to evolve trichromatic vision be the one that eats the least amount of fruit? It didn't make a lot of sense."

In a 1997 publication, Lucas noted that young red leaves are an important food resource for macaques in Southeast Asia. Compared with mature leaves, the red ones are more easily digested and contain more protein. Dominy, at the time a graduate student working with Lucas, then surveyed the widely varying diets of African primates.

"What I found was that they all--even the chimpanzee, which eats the most fruit--rely upon leaves at critical points in the year, and that when they do that they are relying on the youngest leaves, which are reddish in color," says Dominy. He and Lucas reported the data in 2001, claiming confirmation that trichromacy originally evolved for picking out the most nutritious leaves and not for finding ripe fruit.

Some investigators, such as a group headed by John D. Mollon of University of Cambridge in England, land, don't see an either-or situation. "Our conclusion has been that primate color vision is optimized for detecting any target ... against a foliage background," he says.

Other scientists aren't certain anyone will ever know whether primates first used their improved color vision to pick out fruits or leaves or to do something no one has yet guessed. "I think it's one of these fruitless debates," jokes James Bowmaker of University College London, who studies the evolution of vision. "There's no argument that having the red-green color vision we have does enable us to do these tasks, but whether that's why it evolved is another question. And you will never answer that one, of course. You can't go back 35 million years ago and ask a primate."

LOSING BY A NOSE Even as vision researchers wrestle over why trichromacy evolved, other investigators have linked its development in primates to a decline in another sensory system: smell. Many vertebrates have two regions in their nasal cavities that are specialized for detecting airborne chemicals. The first, the main olfactory epithelium, depends upon nasal-cell-surface proteins, called olfactory receptors, to recognize odors. The second sensory region is the vomeronasal organ (VNO). It detects the pheromones that species use to regulate their reproductive behaviors. Rodents, for example, rely upon pheromones to identify willing mates.

Despite the ads for pheromone-based perfumes, there's a controversy over how strongly people respond to pheromones (SN: 10/13/01, p. 232). One of the arguments against the importance of pheromones in people is that the human VNO is a shrunken pit with no obvious functionality. Any residual capability to sense pheromones has probably shifted from the VNO to the main olfactory epithelium, suggests Emily R. Liman of the University of Southern California in Los Angeles.

Curious about when in human evolution the VNO began to atrophy, Liman and her USC colleague Hideki Innan recently examined the DNA of 15 primate species, including both Old World and New World species. Specifically, the researchers were looking at the gene for a protein called transient receptor potential cation channel 2, or TRPC2. According to studies on the rodent version of the gene, it's active only in the VNO, and the cell-membrane protein it encodes is necessary for pheromone detection. Not surprising then, the rodent version of the gene is intact, while the human copy has mutations that render the gene useless.

In the March 18 Proceedings of the National Academy of Sciences (PNAS), Liman and Innan reported that the gene in Old World monkeys and apes also carries disabling mutations. In contrast, they found no serious mutations in the VNO gene in the New World primates they studied. From this, they conclude that the gene, and therefore most likely the VNO, began to deteriorate after the split between New and Old World primates but before the Old World monkeys and apes diverged. That timing approximately coincides with the appearance of the third opsin gene, and therefore trichromacy, in Old World primates.

Essentially, the same conclusion has been reached by Jianzhi Zhang and David Webb of the University of Michigan in Ann Arbor, who report a similar study of the same VNO gene, which they call TRP2, in the July 8 PNAS. Their additional analysis of other VNO genes also dates the organ's decline to shortly before the lineages of Old World monkeys and apes separated, about 23 million years ago.

It could be a coincidence, admits Liman, but she speculates that the improved color vision helped Old World primates recognize a mate in heat and so lessened the need for pheromone detection. Both research teams note that females of Old World primate species have unusual swelling and redness of their bottoms when they're ovulating. This visual signaling of mating readiness, which may have replaced pheromone cues, probably arose only after trichromacy evolved, the researchers say. At that point, random mutations could disable VNO genes without causing a problem.

In addition to losing their capacity to sniff out pheromones, Old Word primates may have begun losing other parts of their sense of smell after they acquired superior color vision. Mammals have more than a thousand genes for olfactory receptors. However, scientists recently found that more than 60 percent of those genes are nonfunctional in people, versus only about 20 percent in mice (SN: 5/6/00, p. 298).

At this summer's Society for Molecular Biology and Evolution meeting in Newport Beach, Calif., Yoav Gilad of the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, reported that Old World monkeys and apes tend to have significantly fewer functional olfactory genes than New World monkeys do. Given that the former all have full-fledged trichromacy, Gilad argued that olfactory-receptor genes, like the genes used to sense pheromones, deteriorated once the primates began to grow more dependent on visual information than on smells. He also noted that New World howler monkeys, with their Old World-style trichromacy, have fewer functional olfactory genes than other New World monkeys do.

The lesson of these recent studies may be that whatever evolution gives to an animal, it can also take away. Indeed, scientists have noted that red-green color blindness is much more prevalent in people than in chimpanzees and other Old World primates. Perhaps because people now turn to the local market for their food instead of foraging among the foliage, they no longer need to see red.

FRUITFUL RESEARCH--The improved color vision of Old World primates may help them find ripe fruit among green leaves.

LEAFY DIET--Young red leaves, eaten by many primates, tend to have more nutritional value and be more easily digested than mature green leaves are.