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Evolution of color vision: transgenic mice see red

This week’s paper, "Emergence of novel color vision in mice engineered to express human cone pigment", by Gerald Jacobs and colleagues at UC Santa Barbara and Johns Hopkins Medical School (Science 315:1723), is yet another experimental study that increases our understanding of how repeated cycles of natural selection, each producing a fairly small change, can lead to adaptations that may seem irreducibly complex.

Most humans have three different photopigment color sensors, as do our closest relatives. Many other mammals, including mice, have only two. Three-color vision is useful for many purposes, from identifying higher-protein leaves to eat (Nature 410:363) to telling which wire to cut to disarm the nuclear bomb buried under the stadium. But eventual usefulness isn’t enough for a trait to evolve. If a series of steps is required, each step must be beneficial, or at least not lethal. Such a series of steps has been worked out for the evolution of optically sophisticated eyes from light-sensitive spots (Proc. Roy. Soc. B 256:53), but what about color vision?

New World monkeys have a form of color vision that may have been a stepping stone between the two-color vision of other mammals and the three-color vision we apes enjoy. One of their photopigment genes is on the X sex chromosome; another is on a nonsex chromosome. Males have one X chromosome (and one Y sex chromosome), so two different color receptors. Females with the same photopigment on both X chromosomes also have only two different color receptors. But "heterozygous" females (with two different X chromosomes), can have two different photopigments on their X chromosomes, plus one on the nonsex chromosome, for a total of three photopigments, each sensitive to different colors of light.

How could this form of three-color vision evolve from the two-color version in other mammals? Although mutation of the photopigment gene on the X chromosome would yield some heterozygous females with three photopigments, I would have thought that three-color vision would have additional requirements (special neurons, etc.). But apparently I would have been wrong.

Jacobs and colleagues genetically transformed mice, adding a human gene for a photopigment not normally present in mice. They then tested color vision in heterozygous females, which had three different photopigments: the two normal mice versions (X and non-X), plus the human version on their second X chromosome. These mice varied in the proportion of the two X-linked photopigments. Those with roughly equal proportions were usually able to tell the difference between colors that looked the same to normal mice. The tests involved distinguishing between differently-illuminated color panels, presumably in exchange for mouse treats.

So specialized neuronal circuitry for each photopigment apparently isn’t essential for at least simple three-color vision. The authors suggest that inactivation of different X chromosomes in different cones in the mouse eyes may have helped the mouse brains learn to distinguish nerve signals linked to photopigments that respond to different colors of light.

Once this simple color vision system was established, further evolution of the nervous system could lead to further improvements, so it seems likely that monkeys have better color vision than these transgenic mice. But why haven't monkeys evolved an ape-like color vision, which works for males as well as females? The required evolutionary changes in the nervous system may be trickier for photopigment genes on nonsex chromosomes. Or maybe the benefits of three-color vision aren’t great enough for natural selection to favor allocation of more brain cells to processing additional color information, except in species with large brains. Or, for monkeys living in troops, maybe there are always enough heterozygous females around to serve as color consultants.

The same issue of Science has 1) a paper showing that fewer genes have been transferred from mitochondria (respiratory organelles descended from intercellular symbionts, and retaining some of their own genes) to the cell nucleus in plants that out-cross (produce seeds with another plant rather than by self-pollination), perhaps because out-crossing can scramble interactions between nuclear and mitochondrial genes, and 2) a report on a virus-defense system in bacteria in which viral DNA from a previous infection is used against new infections, analogous to the vertebrate immune system but using a very different mechanism. As in previous weeks, I haven't seen any papers on "intelligent design" this week, maybe because I've only been looking in scientific journals.

Comments

This is really cool! I'll try to send more student traffic your way from my Evolution class.

Thank you, also, for stopping by my little class blog, and leaving a comment. That meeting in UCLA was indeed really stimulating, and I've got a half-baked blog report on it, which I hope to finish and post over the next few days - our spring break starts Friday!

So, what exactly was the principle hypothesis of the study conducted by Jacobs et al in the paper?

Good question. Remember that a result consistent with a hypothesis doesn't prove the hypothesis -- there could be other hypotheses that make the same prediction -- but a result inconsistent with the hypothesis means it's at least slightly wrong. See: www.plantsciences.ucdavis.edu/denison/pdf/RFD4357.pdf

So, what hypotheses, if any, do you think were disproved by the improved color discrimination in the transgenic mice? How about the statement preceding "I would have been wrong"?

That's a good point. I don't think any hypothesis was disproved, rather I think that Jacobs et al proved their hypothesis that an additional pigment would produce chromatic discrimination and the mammalian brain is plastic enough to make the changes to get new sensory input. However I'm not too sure about the part where the heterozygous female would immediately enjoy a selective advantage. This depends on what he means by immediately. Does he mean as soon as the photopigment was introduced? Or does he mean with time after the brain developed the neurons and mechanisms nessecary to facilitate trichromatic color vision?
Do you think that was the hypothesis? Or do you have any other ideas? Also according to Jacobs how has color perception evolved from non- primates to primates? And how has it genetically differentiated between various primates? Does he talk about this anywhere in the article?

"Immediate selective advantage" means greater chance of survival and reproduction in the first animal with the mutation, as opposed to some future generation with additional complementary mutations. This is important because a mutation that is only beneficial in combination with some other mutation will often die out.

This is a subtle point, but a hypothesis needs to be explanatory, so not every prediction qualifies. And -- very important -- a result consistent with a hypothesis does not prove the hypothesis. (Hypothesis: turning the light off at night makes the sun come up in the morning: I tried it and it worked!) See our paper for more detail on both points.

For answers to your other questions, if you don't have access to a library that gets Science, I bet the authors would email you a copy: jacobs@psych.ucsb.edu

Did the investigators mimic the biological evolution of colour perception using transgenic techniques by creating a line of mice that had most of their X- chromosomal M pigment genes replaced by a human L pigment cDNA? Or did they do more then that?

Assuming one pigment gene per X chromosome, they replaced one of them so that's half, not "most." But apparently the amount of pigment protein made by that gene varied. Only the mice with close to a 50:50 ratio had improved color vision. This seems consistent with their hypothesis that the mice compared the signal from the two types of cone (one from each X chromosome) in their eyes. It would be interesting to see the spatial pattern of gene expression in the eyes. Was "seeing red" really "the top looks brighter"? Anyway, assuming this result holds up when repeated by others, it's a nice example of how something that seems like it wouldn't work without all the parts can still be useful in a primitive form.

I think I am not too sure about the part where the heterozygous female would immediately enjoy a selective advantage. This depends on what he means by immediately. Does he mean as soon as the photopigment was introduced? Or does he mean with time after the brain developed the neurons and mechanisms nessecary to facilitate trichromatic color vision?

[From Ford: Good question. As I recall, benefits really were immediate, somewhat surprisingly, and they had a proposed mechanism to explain why.

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