The genomics of being a raptor

Comparing the genomes of different birds of prey reveals the genetic basis of their predatory lifestyles.

This week, I managed to see a Great Grey Owl (Strix nebulosa). For several weeks, bird watchers reported this species in the Swedish nature reserve Hågadalen. On Monday, I took the bus from my office – the Evolutionary Biology Center in Uppsala – to this forest area. After a brisk walk, I arrived at the location and patiently waited. And sure enough, a few minutes later a Great Grey Owl flew over a meadow and landed on a wooden pole. While enjoying this bird, a second individual suddenly appeared around the corner. It soared past – just a few meters in front of me – holding a freshly killed rodent in its beak. This wonderful experience made me think about the evolutionary history of these magnificent birds. How has natural selection sculpted these deadly raptors? Luckily, several recent studies provided a genomic perspective to this question.

Strix_nebulosa

The Great Grey Owl © Olaf Oliviero Riemer | Wikimedia Commons

 

Birds of Prey

Before we dive into the genomics of raptor-hood, we need to understand that raptors are a mixed bunch. They are divided over three bird orders that are not closely related: Accipitriformes (hawks and eagles), Falconiformes (falcons) and Strigiformes (owls). In technical terms: raptors are polyphyletic (see this blog post for more information on these phyletic terms).

The polyphyletic nature of raptors is important to keep in mind when studying their evolution. Because they arose from different ancestors, some adaptations are probably the result of convergent evolution. However, by comparing the genomes of members from the three raptor orders, we can gain more insights into the large-scale genetic changes that accompany a predatory lifestyle. A recent study in the journal Genome Biology did just that. They compared the genomes of 20 birds of prey to understand the genomics of being a raptor.

raptor_tree

Birds of prey are distributed over three orders: Strigiformes (purple), Accipitriformes (green) and Falconiformes (blue). A recent study compared the genomes of 20 species to understand the genetic underpinnings of being a raptor. From: Cho et al. (2019) Genome Biology

 

Gene Families

There are several ways to investigate the genomic background of certain traits. One way is to study the expansion and contraction of gene families. An expansion suggests that the genes are important for a particular trait, while a contraction indicates that the genes are not necessary. Yun Sung Cho and colleagues compared the sizes of gene families of birds of prey with other non-raptorial species. This comparison revealed that all three bird orders experienced an expansion in gene families associated with “sensory perception of sound, regulation of anatomical structure morphogenesis, postsynaptic density and specialization, and learning functions.” How these gene families relate to specific phenotypes remains to be investigated.

Next, the researchers turned to nocturnal species. They contrasted two night-active bird groups (owls and kiwis) with diurnal birds. This analysis showed that several vision-associated gene families contracted. Interestingly, all nocturnal birds seem to have lost the gene SWS1, a violet/ultraviolet sensitive protein. These birds have thus lost part of their color vision. These findings point to vision-related adaptations to a nocturnal lifestyle. But again, more research is needed to sort out the details.

gene_families.jpg

An overview of the expanding and contracting gene families in the different bird orders. From: Cho et al. (2019) Genome Biology

 

Positive Selection

A second approach to identify the genetic basis of particular lifestyles is to search for genes under positive selection. Here, the widely used dN/dS-statistic comes into play. This statistic is based on the genetic code underlying the translation of genes into proteins. As you might remember from high school, a gene can be divided into codons: three-letter combinations that code for a particular amino acid. For instance, TCC codes for Serine while ACC gives you Threonine.

The genetic code has some redundancy, different codons result in the same amino acid. For example, TCT, TCC, TCA and TCG all correspond to Serine. This means that some mutations will not affect the amino acid sequence (e.g., if TCT mutates into TCC, you still have a Serine in the protein). These mutations are called synonymous mutations (dS). However, other mutations do change the amino acid sequence: When TCC turns into ACC, a Serine is replaced by a Threonine. These are non-synonymous mutations (dN).

Now that we know the difference between synonymous (dS) and non-synonymous mutations (dN), we can combine them. A synonymous mutation will not affect the functioning of a protein and can be considered neutral. A non-synonymous mutation, on the other hand, might change the way a protein works. If the protein improves the new mutation will be selected for and increase in frequency. A gene with more non-synonymous mutations (dN) than synonymous (dS) might thus be under positive selection. By calculating this ratio – dN/dS – for numerous genes, researchers can pinpoint putative positively selected genes.

genetic code

The genetic code has some redundancy (i.e. several codons result in the same amino acid). We can use this information to find gene under positive selection.

 

Nocturnal Life

The analyses of the dN/dS-statistic resulted in a long list of positively selected genes. Let’s look at a few interesting owl-cases. In nocturnal birds, the researchers found several hearing-and vision-related under positive selection. For example, the gene ROH is positively selected in night-active birds. This gene encodes a rhodopsin that enables vision in low-light conditions. Another recent study in the journal Scientific Reports performed a similar analysis on the genome of the Oriental Scops Owl (Otus sunia) and discovered that the gene ALCAM is under positive selection. This gene is associated with retina development in owls. Detailed analyses revealed that ALCAM has two owl-specific mutations that possibly possibly enhances low-light sensitivity. It seems that natural selection has improved the nocturnal vision and other sensory systems in owls to compensate for the loss of color vision (i.e. loss of gene SWS1 mentioned above).

Oriental_Scops_Owl

The Oriental Scops Owl © Rejaul karim.rk | Wikimedia Commons

 

Convergent Evolution

The identify of positively selected genes varied between the different bird orders. Only two genes are under positive selection in all three bird orders (RHCE and CENPQ), while other genes are restricted to only two orders (e.g., SFTPA1 in Strigiformes and Falconiformes; TFF2 and PARL in Strigiformes and Accipitriformes). This low number of shared genes suggests that the different raptor groups followed distinct genetic routes to their predatory lifestyles. Clearly, there are numerous genetic ways to be a raptor.

 

References

Cho, Y.S. et al. (2019) Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles. Genome Biology 20:181.

Zhou, C. et al. (2019). Comparative genomics sheds light on the predatory lifestyle of accipitrids and owls. Scientific reports, 9:2249.

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