If you see the world with only two color-detecting pigments in your eye, as many monkeys do, your sense of smell is very important. But in higher primates, which see with three pigments, the sense of smell is less critical, evolutionary biologists have found -- to the extent that people have lost the use of more than half their odor-detecting genes.
The finding has emerged from analysis of odor-detecting genes in the primate tree, which includes people, monkeys and apes. A large proportion of the genes have become inactive in just those primate species that have developed full color vision, say Dr. Yoav Gilad and Dr. Svante Pääbo of the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany.
The detection of smell begins with special receptors embedded in the surface of the nerve cells in the nose. Humans have more than 1,000 receptor-making genes. But analysis of the DNA sequence of these genes, made possible by the recent decoding of the human genome, shows that about 60 percent of the genes carry a mutation that would render useless the receptor protein they specify.
This is a strikingly higher proportion than the 20 percent of olfactory genes that are inactive in dogs and mice. To get a fix on where in the primate line olfactory receptor genes started to become so dispensable, Dr. Gilad, Dr. Pääbo and their colleagues analyzed a set of olfactory genes in people and 18 other primates.
In apes and Old World monkeys, 30 percent of these genes were inactive; but, with one exception, New World monkeys had lost less than 20 percent, the researchers report in today's issue of The Public Library of Science/Biology.
The exception, the howler monkey, had lost 30 percent of its odor genes, just like the apes and Old World monkeys. And like them, the howler monkey has full color vision, the only New World monkey to have evolved this faculty.
Many New World monkeys have only two opsins, the visual pigments sensitive to particular colors of light. Some 23 million years ago, after the split with New World monkeys, the Old World monkeys and apes acquired a third opsin, sensitive to a different region of the spectrum, and thus gained three-color vision. The howler monkey was lucky enough to duplicate one of its opsin genes some 11 million years ago, putting itself in the three-color vision league.
Better vision may help monkeys distinguish ripe fruit from unripe, or young leaves from old, and thus make them less dependent on the sense of smell. The decline in the sense of smell may not be the direct result of the evolution of color vision, the Leipzig researchers say, but the two factors do seem to be related.
''It's a compelling correlation, to me at least, and what makes it compelling is the howler monkeys,'' said Dr. Gerald H. Jacobs, an expert on primate color vision at the University of California at Santa Barbara.
Dr. Pääbo, with his interest in human evolution, wondered when the process of losing olfactory genes first started. He estimates it began two million years ago, just before the advance represented by the emergence of Homo erectus, a more capable hominid with a larger brain.
The loss of olfactory genes is continuing. Dr. Pääbo has found some people in the in-between state of having inherited an inactive smell gene from one parent and an active version of the same gene from the other parent. ''This is an unusually dramatic example of the fact that our genome is still evolving,'' Dr. Pääbo said.
The inactive one will probably become more common in the population, until it has driven the active version of the olfactory receptor gene into extinction. ''We will probably lose over 100 or more genes in the future,'' Dr. Pääbo said.
Humans are not the only ones in an in-between state. The New World monkeys have only two opsin genes, and males see the world with the help of just two color pigments. But one of the opsin genes lies on the X chromosome; females have two copies of it, males only one.
The X-based opsin has two versions: one responds to long wave light and other to medium wavelengths. If the female New World monkeys are lucky enough to have inherited the long-wave opsin gene from one parent and the medium wave from the other, then they have three-color vision, Dr. Jacobs has found.
But if they inherit the same version of the gene from each parent, they are destined to see the world with two-color vision, just as the males do. The howler monkey broke out of this impasse through a genetic accident that duplicated the X-based opsin gene and allowed howlers of each sex to have three-color vision.
The primate retina seems wired to be able to take advantage of an extra color pigment, but it is not clear if this is true of other animals. Dr. Jacobs said that mice with an extra opsin gene, borrowed from humans, have been engineered by Dr. Jeremy Nathans of Johns Hopkins and that he and Dr. Nathans were trying to figure out whether color vision in the mice was enhanced.
Photo: Compared with other New World monkeys, the howler monkey has fewer odor genes. But unlike them, it has full color vision. (Photo by Tom and Pat Leeson/Photo Researchers Inc.)