Convergent evolution of immune proteins in tits, chickadees, and titmice

These small passerines use similar molecular tricks to detect pathogens.

Convergent evolution is a fascinating phenomenon. It concerns the evolution of similar traits in distantly related organisms. Think of the streamlined bodies of fish-eating penguins and auks, birds that diverged more than 60 million years ago. But such similarities are not only limited to morphological traits, evolution can also converge on the same solutions at the molecular level. For example, whales and bats use the same genes for echolocation.

Convergent evolution on the molecular level can be especially important for proteins involved in immunity. These molecular machines need to detect and fight a wide range of pathogens. It is easy to imagine that organisms exposed to the same bacterial or viral species will converge upon similar defense mechanisms. A recent study in the journal Molecular Ecology tested this idea with the bird family Paridae (tits, chickadees, and titmice).

Convergent evolution of body shape in the extinct Great Auk (left) and the Emperor Penguin (right). Credits: Great Auk © Mike Pennington | Emperor Penguin © Samuel Blanc.

 

Toll-like Receptors

Martin Těšický and his colleagues focused on toll-like receptors (TLRs), proteins that recognize signals derived from pathogens and trigger a signaling cascade that starts the innate immune response (first line of defense against all pathogens) and regulates the consequent adaptive immune response (learned response, specific to a particular pathogen). Toll-like receptors have specific structures (called ectodomains, ECD) that contain a ligand-binding region (LBR) which interacts with pathogenic molecules. Because these protein regions have to recognize a wide range of bacteria and viruses, you can expect strong positive selection for successful toll-like receptors.

The study focused on two receptors that are specialized to recognize different signals: TLR4 binds with lipopolysaccharides from gram-negative bacteria, while TLR5 is specific to flagellin (a protein in the bacterial flagellum). The researchers scanned the protein sequences from 29 tit species for sites under positive selection. Next, they investigated whether these positively selected sites altered the structure and binding capacity of the receptors. For instance, a different amino acid in a certain location might have different molecular properties that affect the functioning of the protein. This approach resulted in four positive selected sites in TLR4 and fourteen in TLR5.

Positively selected sites and functionally important sites of the extracellular ectodomain on the great tit TLR4 (a) and TLR5 (b). Positively selected sites are highlighted in blue or orange, and sites under convergent evolution are indicated with red arrows. From: Těšický et al. (2020) Molecular Ecology.

 

Comparing Trees

Now that we have a list of positively selected sites, we can investigate whether they experienced convergent evolution. This can be done by comparing the phylogeny of the Paridae with the evolutionary trajectories of the different sites. These analyses revealed that three positions in
TLR4 and six positions in TLR5 showed signals of molecular convergence. Hence, different tit species independently evolved similar protein structures to fend off invading pathogens. This finding indicates that these species might have experienced similar ecological conditions with shared bacteria or viruses. However, the researchers reported that “the observed evolutionary convergence was not explained by the selected ecological traits, suggesting that more direct evidence on the composition of the microbial communities interacting with TLRs is needed.” Another evolutionary puzzle to solve.

Convergent evolution in Toll‐like receptor 4 (TLR4) in the Paridae family. The species tree on the left does not match the evolutionary history of a particular protein location on the right. Different tit species converged on the same solution independently. From: Těšický et al. (2020) Molecular Ecology.

 

References

Těšický, M., Velová, H., Novotný, M., Kreisinger, J., Beneš, V., & Vinkler, M. (2020). Positive selection and convergent evolution shape molecular phenotypic traits of innate immunity receptors in tits (Paridae). Molecular Ecology29(16), 3056-3070.

Featured image: Black-capped Chickadee (Poecile atricapillus) © USFWS | Wikimedia Commons

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