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Notwithstanding Grand Claims to the Contrary, Human Color Vision Still Presents a Major Evolutionary Enigma


Stephen Meyer commented earlier on the recent review of Bill Nye's new book in the Wall Street Journal. The reviewer, science writer Nicholas Wade, claims that major strides have been made lately in understanding the evolution of human color vision. Is that true?

Writes Mr. Wade:

A recent paper in the journal PLOS Genetics, for instance, describes the seven DNA mutations that occurred over the past 90 million years in the gene that specifies the light-detecting protein of the retina. These mutations shifted the protein's sensitivity from ultraviolet to blue, the first step in adapting a nocturnal animal to daytime vision and in generating the three-color vision of the human eye. Such insights into nature's actual programming language are surely the most undeniable part of evolution at work.
This makes it sound like scientists have uncovered some plausible evolutionary pathway to evolve a complex new trait. No, they haven't. An article at Science Daily explains that this shift in sensitivity to light is a feature that would require multiple mutations before conferring the requisite advantage:
For the PLOS Genetics paper, the researchers focused on the seven genetic mutations involved in losing UV vision and achieving the current function of a blue-sensitive pigment. They traced this progression from 90-to-30 million years ago.

The researchers identified 5,040 possible pathways for the amino acid changes required to bring about the genetic changes. "We did experiments for every one of these 5,040 possibilities," Yokoyama says. "We found that of the seven genetic changes required, each of them individually has no effect. It is only when several of the changes combine in a particular order that the evolutionary pathway can be completed."1

As the technical paper explains, because none of the seven mutations individually has an effect upon light sensitivity, at least two mutations are needed to confer an advantage: "[W]hen the seven mutations are introduced into mouse S1 individually, none of the individual changes produce any ?max-shift, showing an extreme case of epistatic interactions."2 They even identified two specific mutations that were almost always needed to obtain a significant shift in sensitivity:
21 out of 120 interaction terms show that |?| ? 5 nm, most of which (20 out of 21) reflect significant influences of the interaction between F86L and T93P; in particular, F86L is always involved in generating measurable epistatic interactions2
In other words, (a) at least two mutations are required to get any shift in the sensitivity of the protein to different wavelengths of light, and (b) two specific mutations were required to get significant shifts in sensitivity. Since multiple mutations are needed to obtain the claimed changes, it would take a long time for the traits to arise. This poses a challenge to Darwinian evolution, which banks on conserving immediately useful features. Even the Science Daily article concedes:
Human ancestors, however, needed seven changes and these changes were spread over millions of years. "The evolution for our ancestors' vision was very slow, compared to this fish, probably because their environment changed much more slowly," Yokoyama says.1
Rather than finding that human vision could easily evolve, they found the opposite: an unlikely evolutionary pathway. But even if the evolutionary pathway was a likely one, it still represents only small-scale evolutionary change.

Let's say that they did find a series of stepwise mutations, each of which shift the sensitivity of the protein to new wavelengths of light. Would this represent a major evolutionary innovation? Not at all. The study purports to trace the evolution of this protein from a small primitive mammal ancestor some 90 million years ago to the protein in modern humans. In mice, the protein has a maximum sensitivity to light at the wavelength (?) of 359 nm. In humans the same protein does exactly the same job. However, amino acid differences shift the frequency of light to which it's most sensitive. In humans, ?max = 414 nm. They suppose that the common ancestor of humans and mice had a ?max ? 360 nm. Between the ancestral protein and the modern human protein, that's a difference of just 55 nm.

So at best, we're talking about evolving a protein that does the same job, the only change being that its peak sensitivity to light shifted the wavelength by about 55 nm. This is not a new function. It's the same function with small changes.

The Science Daily article also boasts about this lab's prior exploits in answering evolutionary questions about vision:

In 1990, Yokoyama identified the three specific amino acid changes that led to human ancestors developing a green-sensitive pigment. In 2008, he led an effort to construct the most extensive evolutionary tree for dim-light vision, including animals from eels to humans. At key branches of the tree, Yokoyama's lab engineered ancestral gene functions, in order to connect changes in the living environment to the molecular changes.1
Yokoyama sounds extremely confident that he's got everything right:
The PLOS Genetics paper completes the project for the evolution of human color vision. "We have no more ambiguities, down to the level of the expression of amino acids, for the mechanisms involved in this evolutionary pathway," Yokoyama says.1
But did they really explain how these things happened? Are there really "no more ambiguities"?

In those prior studies, Yokayama looked at genes that confer trichromate vision in certain primates and attempted to use statistical techniques to infer that they were under natural selection. But according to one paper, trichromatic color vision does not necessarily give any selectable advantage: "Contrary to the predicted advantage for trichromats, there was no significant difference between dichromats and trichromats in foraging efficiency..."3 In other words, statistical methods may lead biologists to wrongly believe that certain amino acid sites are functionally adaptive.

Yokoyama's 2008 study in PNAS experimentally identified key amino acid sites in rhodopsin genes which are critical for absorbing light in the retinas of various vertebrates. Because these sites are important for the protein's function, they were thought to be under strong selection pressure. The study used statistical methods to investigate whether they were in fact subject to "positive selection." Not only did they find that "none of these predicted ['positive selection'] sites coincide with those detected by mutagenesis experiments," but those sites that were predicted to be under "positive selection" by statistical methods "do not seem to cause" any important changes in light absorption. The paper concluded, "statistical tests of positive selection can be misleading without experimental support."4

Statistical methods predicted certain amino acid sites were functionally adaptive for human-like vision -- but experimental work showed otherwise. Moreover, the experimental methods identified various amino acid sites that were important to the protein's function, but those were not found to be under "positive selection" by the statistical methods. A 2009 paper by Nei et al. in PNAS heavily critiqued Yokoyama's work. They noted that statistical methods for inferring natural selection are "not useful for identifying adaptive [amino acid] sites."5 They conclude: "It is important not to be overenthusiastic about statistical signatures of positive selection without biological confirmation."5 I've written a lengthy review of problems with trying to use statistical methods for inferring natural selection in genes here.

So it's not entirely clear if the claimed amino acid changes leading to the evolution of human trichromate vision were adaptive, nor is it clear if the supposedly selected amino acid changes conferred any benefit. In explaining the evolution of human color vision, it sounds to me like there are many "ambiguities" in this evolutionary story.


(1) http://www.sciencedaily.com/releases/2014/12/141218210100.htm

(2) Shozo Yokoyama, Jinyi Xing, Yang Liu, Davide Faggionato, Ahmet Altun, William T. Starmer, "Epistatic Adaptive Evolution of Human Color Vision," PLOS Genetics (Dec. 2014), Vol. 10 (12): e1004884, http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1004884

(3) Chihiro Hiramatsu, Amanda D. Melin, Filippo Aureli, Colleen M. Schaffner, Misha Vorobyev, Yoshifumi Matsumoto, Shoji Kawamura, "Importance of Achromatic Contrast in Short-Range Fruit Foraging of Primates," PLOS One, Vol. 3: e3356 (October, 2008).

(4) Shozo Yokoyama, Takashi Tada, Huan Zhang, and Lyle Britt, "Elucidation of phenotypic adaptations: Molecular analyses of dim-light vision proteins in vertebrates," Proceedings of the National Academy of Sciences USA, Vol. 105: 13480-13584 (September 9, 2008).

(5) Masafumi Nozawa, Yoshiyuki Suzuki, and Masatoshi Nei, "Reliabilities of identifying positive selection by the branch-site and the site-prediction methods," Proceedings of the National Academy of Sciences USA, Vol. 106: 6700-6705 (April 21, 2009).

Image credit: etrenard/Flickr.