Male squirrel monkeys made to see in living color

Squirrel monkey in Bolivia. Photo: author

Squirrel monkeys, like many New World Monkeys, are a bit unusual when it comes to their vision. Males are dichromatic, meaning that they do not have the ability to see red wavelengths but can see blue and green wavelengths. Females on the other hand, may be dichromatic or they may be trichromatic like us, able to see blues, greens, and reds. Males are dichromatic because trichromatic vision requires two copies of a certain opsin gene, a gene that is found on the X chromosome. Thus, females, who have two Xs, likely (but not always) carry two copies of the gene. The majority of female squirrel monkey can see shades of green and shades of red. Male monkeys have the gene that codes for seeing green colors but not the gene that allows them to see red.

When we refer to color blindness in humans, often what we really mean is that the person has dichromatic color vision. True color blindness in humans, where the person can only see in black and white, is very rare, although something similar does occur in another New World Monkey. Night monkeys have very poor color vision. As their name suggests, these monkeys are active only at night. Thus, seeing reds, greens, and blues isn't very advantageous given their environment. Over time, owl monkeys have evolved so that they have fewer cones, which allow the eye to see colors, and more rods, which allow the eye to distinguish blacks and whites. To further adapt for their mainly nocturnal lifestyle, the size of their eyes has also expanded. Again, being monochromatic is rare in humans, yet dichromatic color vision does occur in one out of twelve men.

Visible Wavelengths Dichromats lack red cones

Now, there may be hope for those who have dichromatic color vision and it's thanks to research done in squirrel monkeys. Two male squirrel monkeys have been made to see all three wavelengths.

Mancuso and colleagues injected the gene that would allow two male squirrel monkeys to see red into a virus, and then they injected that virus behind the retina. (Review your eye anatomy here.) Two years later, the monkeys have had no side effects and are able to see all three wavelengths. Squirrel monkey brains, like our own, are quite plastic, meaning they can change. These two animals can now distinguish reds from greens and their brains have apparently rewired themselves so that seeing and processing information about the red wavelength can be done.

Why do humans see in all three colors? There isn't a certain answer. Multiple hypotheses have been proposed. Peter Lucas, my former professor, believes our ability to see reds was advantageous in helping our ancestors see young red leaves, which are especially nutritious, against a background that is mostly made up of shades of green (Lucas et al., 1998). Our closest living relatives, chimpanzees and gorillas, consume a diet mainly composed of leaves. Or perhaps we see reds because red fruit is often ripe and therefore we can distinguish ripe  fruit against a green background (Allen, 1879; Mollon, 1989; Fleagle, 1999). Yet, if this were the complete answer, wouldn't we expect New World Monkeys, who consume fruit, to see red wavelengths? Another hypothesis suggests that our ability to see shades of red occurred so that male Old World Monkeys could more easily discern the sexual swellings of females that were in estrous (Liman and Innan, 2003).

Regardless of why trichromatic vision evolved in our ancestors, it seems that those humans unable to see all three wavelengths may one day be able to enjoy the Christmas colors following gene therapy. Trials in humans are underway and we have two male squirrel monkeys to thank for that.


Links of interest:
Color vision in primates
Color vision in humans 
Night monkeys and their morphology
A molecular view of how human color vision evolved


Works cited:
 Allen, G. 1879.  The colour-sense: its origins and development. Trubner, London.
Fleagle, J. G. 1999. Primate adaptation and evolution. 2nd ed. Academic Press, San Diego, CA. 

Liman, E. R., & Innan, H. (2003). Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proceedings of the National Academy of Sciences, 100(6), 3328-3332

Lucas, P. W., Darvell, B. W., Lee, P. K. D., Yuen, T. D. B., & Choong, M. F. 1998. Colour cues for leaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestion for the evolution of trichromatic colour vision. Folia Primatologica, 69(3), 139-154.

Mancuso, K. et al. Nature advanced online publication, doi:10.1038/nature08401 (2009). 

Mollon, J. D. 1989. “Tho'she kneel'd in that place where they grew…” The uses and origins of primate colour vision. Journal of Experimental Biology, 146(1), 21-38.

Female orangutans may prefer males with large cheekpads

Dominant male named Kiko at NZP. Photo: author

Orangutans display an interesting form of sexual dimorphism in that males have large cheek pads but females do not. Males are also larger and have large throat sacs that aid them when they make long calls, which advertise to females and tell other orangutans, "I am here!" However, not all males develop this large size, cheek pads, and throat sac. The cheek pads, large size and throat sacs are characteristic of dominant males. Thus, orangutan males display bimaturism, meaning the timing of development differs. Some males develop these dominant characteristics much sooner than others.  Because adult males aren't always large and with the distinguishing cheek pads and throat sacs, it can be quite difficult to tell non-dominant males and females apart.


These non-dominant males aren't juvenile or infertile. They are perfectly capable of reproducing and previously have been shown to produce about half of all wild orangutan offspring (Utami et al., 2002). These two forms of adult males have different strategies when it comes to mating. The dominant males defend their territory. Their homerange is very large and includes multiple females. Non-dominant males are able to gain access to females when the dominant male isn't around.

Bonnie(female) at NZP. Photo: author

A new study resulting from eight years of field research at Tanjung Puting National Park on the island of Borneo found that females prefer dominant males with cheek pads. This is the longest study to have been done at one site in a single population of individual orangutans in terms of orangutan paternity. Banes and colleagues (2015) determined parentage for orangutans inhabiting the homerange used by Kuasasi, a dominant male. They determined he produced far more offspring once he achieved dominance and that he fathered the majority of offspring in the area. This is in contrast to what Utami and colleagues found in 2002 in Sumatra in which unflanged males produced half of the offspring.

This more recent study is arguably limited by the fact that researchers determined the parentage of orangutans in one dominant male's range (Kuasasi). It is possible this is just one very successful male. Or, females are in fact choosing dominant, flanged males over unflanged males. The authors also point out that their study site may affect their results. Camp Leakey is characterized by both wild orangutans and individuals that were once captive but released to the area in the 70s. Orangutans at this site also receive medical treatment, which may mean that dominant males are surviving attacks that they otherwise would not, affecting the population.

Conducting studies on paternity and life history variables on orangutans is very difficult given that, other than humans, orangutan offspring take the longest to reach adulthood of any primate. Females will reproduce every eight years (Gladikas and Wood, 1990), thus answering these types of questions remains difficult.

Links of interest:
Encyclopedia of Life Page on Bornean Orangutans
 IUCN Redlist Page on Bornean Orangutan
Monopoly of the male orangutan
Orangutan long call


Sources:

Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191

Graham L. Banes, Biruté M. F. Galdikas, Linda Vigilant. Male orang-utan bimaturism and reproductive success at Camp Leakey in Tanjung Puting National Park, Indonesia. Behavioral Ecology and Sociobiology, 2015; DOI: 10.1007/s00265-015-1991-0

Utami, S. S., Goossens, B., Bruford, M. W., de Ruiter, J. R., & van Hooff, J. A. (2002). Male bimaturism and reproductive success in Sumatran orang-utans. Behavioral Ecology, 13(5), 643-652.