The genomics of being an owl

The search for candidate genes leads to a surprising hypothesis.

Owls are beautifully adapted for a predatory lifestyle in the dark. Their big eyes contain a duplex retina that is dominated by rods, the photoreceptors that are sensitive to light. The asymmetrical position of their ears and their flat facial disk give the owls a superior sense of hearing. And their soft feathers ensure a silent flight, allowing owls to sneak up on unsuspecting prey. The morphological adaptations of these nightly birds are well-studied, but the genetic basis of these traits remains largely unknown. In a recent Genome Biology and Evolution paper, Pamela Espíndola-Hernández and her colleagues used a genomic approach to identify the genes underlying these adaptations.

Substitutions

The researchers compared the genomes of eleven owl species with nine other bird species. At the base of the owl-clade, they counted the number of nonsynonymous and synonymous substitutions. Nonsynonymous substitutions lead to a change in the protein sequence (i.e. another amino acid) and are often subjected to natural selection. Synonymous substitutions do not change the protein sequence due to the redundancy in the genetic code (see this blog post for more details on the genetic code). Because these synonymous changes to not affect the protein sequence, they are generally not picked up by natural selection. By estimating the ratio of nonsynonymous (dN) to synonymous (dS) substitutions in a gene, evolutionary biologists can detect genes under positive selection. A dN/dS ratio bigger than 1 corresponds to more nonsynonymous substitutions in a gene and points to strong positive selection.

Using this approach, the researchers were able to create a list of candidate genes subjected to positive selection in the owl genomes. After correcting for the multiple statistical tests, 22 candidate genes remained. A functional analysis of these genes revealed that they were mostly related to “detection of stimulus involved in sensory perception.” This result points to genes involved in the auditory and visual adaptations of owls. Among others, we come across the genes TMC2, which is involved in the workings of cochlear hair cells of the inner ear, and PPEF2, which is expressed specifically in photoreceptors. Interesting targets for further research.

An overview of several candidate genes and their functional pathways. These networks highlight genes involved in vision and chromosome condensation.

Light-collecting Lenses

The discovery of genes involved in vision and hearing were expected, but the analyses also uncovered another set of genes were under positive selection: those involved in chromosome condensation. This finding suggests that owls might have evolved a special type of DNA packaging in the retina, similar to what has been reported in nocturnal mammals. In most eukaryotic cells, the condensed DNA (i.e. heterochromatin) is located at the nuclear periphery and the lightly packaged DNA (i.e. euchromatin) is found at the nuclear interior. In the rods of nocturnal animals, however, this pattern is reversed, which turns the rod nuclei into light-collecting lenses. Computer simulations showed that columns of such nuclei channel light efficiently toward the light-sensing rods. Whether the same mechanism applies to the eyes of owls remains to be determined, but is certainly an exciting hypothesis to test. This result highlights the value of genome-wide quests for candidate genes, which can lead to surprising insights or new research lines.

The different arrangement of DNA in the cells of nocturnal mammals (figure K) might channel light more efficiently to the light-sensitive rods in the eye. From: Solovei et al. (2009) Cell.

References

Espíndola-Hernández, P., Mueller, J. C., Carrete, M., Boerno, S., & Kempenaers, B. (2020). Genomic evidence for sensorial adaptations to a nocturnal predatory lifestyle in owls. Genome Biology and Evolution12(10), 1895-1908.

Featured image: Eurasian Eagle-Owl (Bubo bubo) © Rhododendrites | Wikimedia Commons

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