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Mammals' nocturnal past shapes sun sensitivity

September, 2015
By guest author Christopher A. Emerling, PhD, NSF Postdoctoral Fellow, UC Berkeley Museum of Vertebrate Zoology

Sunburnt shoulders

As you soak up the last rays of the summer sun, here's something to think about: if it weren't for a quirk of our mammalian evolutionary past, your body could probably produce its own sunscreen. Back in May, researchers reported that they had discovered a mechanism by which zebrafish can generate a non-pigment-based sunscreen compound known as gadusol. They also found that the genes encoding the pathway for gadusol production are widespread; they are present in other fish species, as well as in amphibians, reptiles, and birds. This suggests that these genes arose early in vertebrate history and were passed down to many descendant lineages. This discovery is somewhat unsurprising, however, given the fact that all animal tissues are susceptible to damage from ultraviolet radiation. The protection these genes offer could represent a significant survival advantage. What is surprising about the new research is that the genes are completely absent in mammals. If our closest vertebrate relatives retained the genes for gadusol production, why didn't mammals as well? The answer may lie in our deep evolutionary past, just as the mammalian lineage was arising...

Where's the evolution?

Mammals are part of a lineage of animals called synapsids that descended from reptile-like ancestors. Some examples of non-mammalian synapsids include the sail-backed Dimetrodon and the herbivorous dicynodonts. Despite our shared reptilian ancestry with lizards, turtles and birds, the eyes of mammals are very unlike theirs. In particular, mammalian eyes seem to have adaptations for seeing well at night, even in species that are active during the day. For example, mammals have especially large corneas relative to their eye size, which is more similar to nocturnal lizards and birds than to their light-loving counterparts. Possessing a large cornea allows for more light to be captured, an important trait for living in dim light conditions.

phylogenetic tree

Researchers have also inferred that mammals had a long nocturnal past based on the loss of various genes related to light reception. For example, mammal color vision is greatly reduced compared to our reptile and bird cousins, a feature that likely reflects the fact that color receptors work best in bright light. Whereas the typical reptile and bird possesses genes encoding four different types of color receptors, the earliest mammals only retained two color receptor genes. The ancestor to apes, macaques and baboons duplicated one of these genes, so humans inherited a third receptor type, but we still can't quite see the diversity of colors that lizards, turtles, and birds can. Mammals also lost genes related to other types of photoreception, such as some that help shape circadian rhythms. Out of 11 non-visual photoreceptive genes typical of amphibians, reptiles, and birds, mammals only retain five to six.

So, how exactly, did mammals "lose" all these genes? Loss of gene function can happen in many ways, but all involve the process of mutation. With every generation, lineages experience random mutation. The effects of these mutations vary from harmful to neutral, or occasionally advantageous. Some of these mutations may "break" a gene, disrupting its operation. Such loss-of-function mutations can involve a single change in a base of DNA or a rearrangement of large chunks of the genome. One scenario for gene loss involves a single mutation that disrupts the function of a gene. This mutation prevents the gene from being translated correctly, leading to the absence of the trait. Of course, if the affected gene is important for survival and reproduction, the "broken" version of the gene will be weeded out of the population through natural selection. However, if the gene is not important for survival and reproduction in the population's current environment — as would likely be the case for a sunscreen gene in a nocturnal lineage — the "broken" version of the gene may be passed on to offspring and spread. Sometimes the accumulation of disruptive mutations in a gene can be followed by its complete deletion from the genome.

During mammals' so-called "nocturnal bottleneck," we lost many genes — and now we know that the genes for gadusol production were among them. Based on the new research, which found that these genes were missing in all 39 of the mammal species examined, the genes appear to have been completely deleted from the ancestral mammalian genome. Since early mammals were active during the night, they were only very rarely exposed to the intense ultraviolet radiation of the sun. When loss-of-function mutations arose in the genes that offered UV protection, natural selection would not have weeded these mutations out. After all, what use is sun protection when you only are exposed to the moon and stars? Instead, the mutations accumulated, wiping out the gene entirely. As a result, humans, along with all of our furry cousins, can no longer produce this sunscreen compound. However, we do still produce melanin — a pigment-based sunscreen that is responsible for dark skin, which also has other functions like providing coloration for camouflage and species recognition. Nevertheless, even with melanin, we are presumably more sensitive to UV damage than we might have been had our ancestors not lost the genes encoding gadusol production. Interestingly, the researchers who discovered this natural sunscreen in zebrafish also demonstrated that when these genes are inserted into yeast, they produce gadusol, providing UV protection for the yeast. Someday this method might be used to manufacture an all-natural sunscreen. If such an industry ever develops, you'll be able to get in touch with your inner fish by slathering on the compounds that you lost the ability to produce some 200 million years ago.


Read more about it

Primary literature:

  • Osborn, A. R., Almabruk, K. H., Holzwarth, G., Asamizu, S., LaDu, J., Kean, K. M., ... Mahmud, T. (2015). De novo synthesis of a sunscreen compound in vertebrates. eLife. 4: e05919.
    read it
  • Hall, M. I., Kamilar, J. M., and Kirk, E. C. (2012). Eye shape and the nocturnal bottleneck of mammals. Proceedings of the Royal Society of London B: Biological Sciences. rspb20122258.
    read it
  • Gerkema, M. P., Davies, W. I., Foster, R. G., Menaker, M., and Hut, R. A. (2013). The nocturnal bottleneck and the evolution of activity patterns in mammals. Proceedings of the Royal Society of London B: Biological Sciences. 280(1765): 20130508.
    read it
News articles:

Understanding Evolution resources:

Discussion and extension questions

  1. The genes for gadusol production are widespread among vertebrate species. What does this fact suggest about when and in which lineage these genes arose? Explain your reasoning.
  2. In your own words, explain why mammals don’t carry the genes for gadusol production.
  3. What evidence suggests that the ancient mammals went through a significant period during which they were nocturnal? Describe three lines of evidence.
  4. Imagine that a classmate reads the article above and then says that birds and reptiles needed gadusol for sun protection, so their genes for gadusol production didn’t mutate. How would you correct his statement?
Related lessons and teaching resources

  • Teach about gene loss: This short video from HHMI for grades 6-16 describes how scientists have pieced together the evolutionary history of the Antarctic icefish by studying its genome — an excellent case study on genetic evolution as both the gain and loss of genes have led to key adaptations.
  • Teach about mutation and natural selection: In this activity from the NIH for undergraduates, students use data and the principles of natural selection to explain the relatively high frequency of alpha-thalassemia in certain populations. They also learn how comparisons of genetic sequences help researchers studying cleft lip and palate, as well as how natural selection has conserved the genetic sequences responsible for these defects.
  • Teach about the evolution of color vision : This case study from Evo-Ed for undergraduates comes in the form of a set of PowerPoint slides and examines the evolution of trichromatic vision in old world monkeys.

References

  • Osborn, A. R., Almabruk, K. H., Holzwarth, G., Asamizu, S., LaDu, J., Kean, K. M., ... Mahmud, T. (2015). De novo synthesis of a sunscreen compound in vertebrates. eLife. 4: e05919.
  • Hall, M. I., Kamilar, J. M., and Kirk, E. C. (2012). Eye shape and the nocturnal bottleneck of mammals. Proceedings of the Royal Society of London B: Biological Sciences. rspb20122258.
  • Gerkema, M. P., Davies, W. I., Foster, R. G., Menaker, M., and Hut, R. A. (2013). The nocturnal bottleneck and the evolution of activity patterns in mammals. Proceedings of the Royal Society of London B: Biological Sciences. 280(1765): 20130508.


Image of sunburnt woman by Flickr member Kevin O'Mara.