Evolution plays visual leapfrog: Ultraviolet to violet

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  • Published: Oct 1, 2015
  • Author: David Bradley
  • Channels: UV/Vis Spectroscopy
thumbnail image: Evolution plays visual leapfrog: Ultraviolet to violet

You say you want evolution

The African clawed frog ran an evolutionary competition with its eye's pigment molecules allowing it over the millennia to develop violet as from UV vision.

There is nothing odd about an animal such as the African clawed frog, Xenopus laevis, which just happens to lack a tongue, has long, curved toes and eyes perched atop its head, except perhaps for one thing...the frog's evolutionary ancestors had ultraviolet vision, but the modern species ditched that app for violet vision instead. Bizarrely, and one has to admit this really is odd, the evolutionary pressure on those molecules of vision kept trying to leap over each other to get ahead, but other molecules would shut them down thus slowing the transition from ultraviolet vision to violet to something of a crawl.

Now, Shozo Yokoyama, a biologist at Emory University, Atlanta, Georgia, USA, who specializes in adaptive evolution of vision and colleagues Huiyong Jia, Takashi Koyama, Davide Faggionato and Yang Liu as well as Ahmet Altun of Faith University in Istanbul, Turkey and William Starmer of Syracuse University in New York, USA, have published details of this astonishing molecular tale in the journal Science Advances.

"It's the most bizarre, and sophisticated, case of colour vision evolution that I've ever encountered," Yokoyama says. Previously, he led efforts to construct the most extensive evolutionary tree for vision, including 500 species of animals, from eels to humans. "This frog had these quirks for rapid molecular change, but it also had something to control these quirks," he says. "In fact, it had triple protection."

There are five classes of opsin genes that encode for the visual pigments for dim-light and colour vision. Components of these genes can mutate and allow vision to adapt as a species evolves. Ultraviolet (UV) vision gives a bi-chromatic, high-contrast view of the world that can be useful for many patterns of animal behaviour. For instance, voles that mark their territory with urine or faeces can see the patches left by themselves and others in their territory. Violet or blue light vision gives an animal a more detailed view of a scene, they get higher resolution. It is possible that the African clawed frog transitioned from UV to violet sensitivity may have been a reproductive adaptation wherein it could see potential mates better in the blue region of the spectrum rather than beyond. Conversely, or perhaps additionally, the same adaptation may have made it easier for the frog to discern predators better, a green snake among green leaves, for instance.

The paths to violet vision

Yokoyama's earlier work on X laevis had identified some of the genetic mutations involved in the process of the frog’s switch from UV vision to its current function of violet vision. For instance, he and his colleagues had shown that amino acid residue 113 on the pigment had switched from glutamic acid to aspartic acid. "Of all the species in the animal kingdom that have been studied, site 113 is made up of glutamic acid, but this frog had changed site 113 to aspartic acid," Yokoyama explains. "Why did it do that? This question was very mysterious and interesting to me. What is so special about this frog?"

Yokoyama's experiments are lengthy involving as they do teasing out the secrets of adaptive evolution by first estimating and then synthesizing ancestral proteins and pigments for a given species, and then testing them to see how those proteins behave and uncovering differences with the natural "modern" proteins. Their approach combines microbiology, theoretical calculations, biophysics, quantum chemistry and genetic engineering. In the current work on X laevis, the team identified the twelve mutations that were involved in the frog's vision shift. These twelve molecular changes could have 500 million possible combinations of pathways that connect the ancestral UV vision and the modern frog's violet vision. So, the team narrowed down their search for clues to the changes that have occurred in the six layers of transmembranes in which these twelve molecules are located. This sharpened focus reduced the number of possible evolutionary pathways from half a billion to a slightly more manageable 720.

Colourful leapfrog

With this reduced number of pathways to investigate, the team then assembled molecular "chimeras" comprising the ancestral and modern frog pigments for all of these pathways. They then tested to see how the molecules functioned in all the different combinations, to home in on the correct pathway. Ultimately, their results showed that the mutations that occurred on transmembranes four, five and six happened early during the evolutionary process from frog ancestor to modern X laevis. It was, however, much later that these mutations came into play in. The mutations occurring on transmembrane two caused small shifts in the range of the light spectrum that the pigment detected. The mutations occurring early in evolution on transmembrane three, however, where amino acid 113 resides, led to a huge leap in the wavelength sensitivity from 400 to 600 nanometres.

Three times, molecules on transmembrane three mutated to cause a big jump toward violet sensitivity. The first time it happened, transmembrane five came into play, shrinking the molecular structure of the pigment and making it non-functional. The second time that transmembrane three mutated, launching another leap, transmembrane six sprang into action, again shrinking the molecular structure. The third time transmembrane three tried to make the evolutionary leap, number four shut it down by destroying a critical chemical structure of the pigment.

The team suggests that the frog pigment essentially slowed during the early evolutionary process for the mutations from glutamic acid to aspartic acid at site 113. Only towards the end of the process did the pigment accept the site 113 shifts. At this point the wavelength leap was not so much a leap as a small step for a little frog of a mere 15 nanometres.

"The human process for evolving from UV to violet vision was far more simple and straightforward," Yokoyama explains. "The story of this frog is full of mysterious twists and turns. A series of strange coincidences happened at the right time, at the right spot, for the right species."

Related Links

Sci Adv 2015, 1, e1500162: "Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions"

Article by David Bradley

The views represented in this article are solely those of the author and do not necessarily represent those of John Wiley and Sons, Ltd.

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