How did snowfinches adapt to high-altitude environments?

Were the adaptations already present in the ancestor or not?

In the Origin of Species, Charles Darwin succinctly defined natural selection as the “preservation of favorable variations and the rejection of injurious variations.” This seemingly simple mechanism has given rise to a mind-boggling array of adaptations. However, the exact series of events leading up to an adaptation is often difficult to reconstruct. This issue is especially apparent in groups of closely related species that show the same adaptations. Were these traits already present in a common ancestor or did the species independently evolve these similarities? A recent study in the journal PNAS addressed this question for snowfinches, an assemblage of closely related passerines that have successfully adapted to life at high altitude on the Qinghai-Tibet Plateau. Several adaptations (such as a more efficient metabolism) have been described in great detail, but the underlying evolutionary history remains to be unraveled.

Positive Selection

A large team of Chinese scientists sequenced the whole genomes of three species: the White-rumped Snowfinch (Onychostruthus taczanowskii), the Rufous-necked Snowfinch (Pyrgilauda ruficollis), and the Black-winged Snowfinch (Montifringilla adamsi). Comparing these genetic sequences with several lowland species, such as the Eurasian Tree Sparrow (Passer montanus), allowed the researchers to identify genes under positive selection in the three snowfinch species and their common ancestor. These analyses revealed that about 95% of the positively selected genes (PSGs) differed between the ancestor and descendant species. Moreover, these genes tend to perform drastically different functions. For example, PSGs in the Black-winged Snowfinch are mainly involved in developmental processes, whereas PSGs in the Rufous-necked Snowfinch largely play a role in cellular processes.

Despite these species-specific patterns, some high-altitude adaptations were probably already present in the ancestor. Specifically, the analyses indicated signs of positive selection in genes related to certain developmental processes, cellular signaling and DNA repair systems. Taken together, the researchers concluded that “After initial adaptation in the ancestor, the descendant species have adapted divergently in response to local selective pressures and microhabitats unique to each species, leading to a deviation of adaptations between the ancestor and each of its descendants.”

An overview of positively selected genes (PSG) in three snowfinches and their common ancestor. Analyses of the gene functions revealed significant differences between the ancestor and its descendants. From: Qu et al. (2021).

DNA Repair

To identify genes under positive selection, the researchers partly relied on the ratio between synonymous and nonsynonymous substitutions. Synonymous substitutions do not change the amino acid in the protein sequence due to the redundancy in the genetic code (see this blog post for more details on the genetic code). Hence, these substitutions are generally assumed to be neutral. Nonsynonymous substitutions, however, do lead to a change in the protein sequence which can affect the function of the protein and subject it to natural selection. A gene with more nonsynonymous than synonymous substitutions might thus be under positive selection.

However, a recent study in the journal Nature questioned the neutral nature of synonymous substitutions. Experiments with yeasts revealed that three-quarters of synonymous mutations resulted in a significant fitness reduction. Whether these results can be extended to other organisms remains to be investigated. Indeed, evolutionary dynamics on the molecular level can be drastically different between single-celled yeast and vertebrates, such as birds. Nonetheless, one should always be careful with interpreting the ratio between synonymous and nonsynonymous substitutions. It is only one indication for positive selection. The best strategy is to perform multiple tests to figure out if a gene has been positively selected.

And that is exactly what the researchers in this study did. They focused on DTL, a gene that is possibly under strong positive selection in the snowfinches. This gene plays a role in the repair of UV-induced DNA damage, an important feature when living at high altitude where UV-radiation can be intense. The researchers chemically synthesized the genetic sequences for the DTL-gene in all three snowfinches species, their ancestor and a lowland species (the Eurasian Tree Sparrow). Experiments with the synthetic genes revealed that the DNA-repair capacity of the snowfinch-genes was significantly better than the lowland-version. These results are thus in line with the assumption that DTL has been under strong positive selection in the snowfinches. A great example of how use different lines of evidence to support a conclusion.

Experiments with synthetic DTL-genes indicated that the snowfinch-versions (in different colors) are more efficient compared to a lowland-version (in black). The two graphs represent different ways of quantifying DNA-damage repair based on their molecular products (6-4PP and CPD). From: Qu et al. (2021).

References

Qu, Y., Chen, C., Chen, X., Hao, Y., She, H., Wang, M., … & Lei, F. (2021). The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai–Tibet Plateau. Proceedings of the National Academy of Sciences118(13), e2012398118.

Shen, X., Song, S., Li, C., & Zhang, J. (2022). Synonymous mutations in representative yeast genes are mostly strongly non-neutral. Nature, 1-7.

Featured image: Rufous-necked Snowfinch (Pyrgilauda ruficollis) © Dibyendu Ash | Wikimedia Commons

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