Are primates at risk of COVID-19?

The emergence of the novel coronavirus SARS-CoV-2 is highly infectious in humans, and the ensuing disease, COVID-19, has caused more than one million deaths. Using comparative genetics and protein-protein interaction modeling we predict many of our closet living relatives are also at risk.
Published in Microbiology
Are primates at risk of COVID-19?

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Amidst the massive global disruption and loss of life caused by the emergence and spread of SARS-CoV-2, my coauthors and I, like so many others, were overwhelmed by a myriad of concerns about the safety of our families and friends while struggling to carry on our academic responsibilities. At the same time, we also became increasingly concerned for the nonhuman primates at our field sites and around the world.

From left to right: Melin observing white-faced capuchins in Sector Santa Rosa, Costa Rica; Janiak observing primates at La Suerte Field Station, Costa Rica; Higham with rhesus macaques on Cayo Santiago, Puerto Rico.

Nonhuman primates are our closest living relatives. Unfortunately, many species are threatened, endangered, or critically endangered, and found in small population sizes.  We anticipated that due to our close evolutionary history, shared physiology, and given previous evidence of zoonotic transfer of respiratory viruses, that nonhuman primates would likely also be at risk of COVID-19. Many primatologists and conservation biologists shared these concerns and on March 15, 2020, the International Union for the Conservation of Nature (IUCN), together with the Great Apes section of the Primate Specialist Group, released a joint statement with recommendations for precautions that should be taken when interacting with great apes. However, the nature of the risk to many primate taxa was unknown. In an effort to provide information to decision makers at all levels, we investigated the likelihood of initial susceptibility to SARS-CoV-2 infection for different major radiations and species. 

A male drill, one of the many critically endangered primates likely to be susceptible to infection by SARS-CoV-2. Photo credit James P Higham.

We worked long (and creative) hours over the next week, motivated to share our results with the community in a timely manner. We coordinated research efforts, writing, sharing, and carefully reviewing results while in lockdown in two countries using Whatsapp, Zoom, and Google Docs to facilitate the conversation and our teamwork. Our approach combined comparative genetics and protein-protein interaction modeling to predict binding affinity for SARS-CoV-2 to the viral target receptor, ACE2, which is expressed on cell surfaces across the body. 

Model of human ACE2 in complex with SARS-CoV-2 receptor binding domain. Key ACE2 interfacial residues are highlighted.

We found high conservancy in the amino acid sequence of ACE2 receptor protein among apes and all monkeys in Africa and Asia (parvorder Catarrhini) including uniformity at all identified and tested major binding sites. These results strongly suggest that these primates are likely to be susceptible to infection by SARS-CoV-2.

ACE2 protein sequence alignment and evolutionary relationships of study species

We were surprised to find potentially better news for monkeys in the Americas (parvorder Platyrrhini) and tarsiers. Differences in amino acid residues at binding sites are modeled to reduce the binding affinity between SARS-CoV-2 and ACE2 by ca. 400-fold.

Interactions at critical binding sites 41 and 42 are shown for the residues found in all catarrhines (apes and monkeys in Africa and Asia; left) and for the residues found in all platyrrhines (monkeys in the Americas; right). The dashed lines indicate predicted hydrogen bonding interactions. Tyrosine (Y) at site 41 participates in extensive van der Waals and hydrogen bonding interactions with receptor binding domain (RBD); these interactions are abrogated with histidine (H). Glutamine (Q) 42 side chain amide serves as a hydrogen acceptor and donor to contact RBD; change to glutamic acid diminishes the hydrogen bonding interactions.

In contrast to the widespread conservancy we observe within the Catarrhini and Platyrrhini, we find greater variation at the critical binding sites of lemurs. Species such as the aye-aye, which possess the human-like amino acid (Y, tyrosine) at site 41, are predicted to be at greater risk than species with histidine (H) at this site, including mouse lemurs. 

Aye-ayes (left) are predicted to have greater susceptibility than  mouse lemurs (right) to infection by SARS-CoV-2. Photo credit to David Haring (left) and Malcolm Ramsay (right).

Overall, while some species are modeled to be at lower risk than humans, we urge extreme caution in using our analyses as the basis for relaxing policies regarding the protection of platyrrhines, tarsiers or any strepsirrhines. With many primates existing in small populations, the introduction of a new highly infectious disease is a critical threat. Our results suggest that dozens of nonhuman primate species, including all of our closest relatives - the monkeys and apes in Africa and Asia - are likely to be highly susceptible to SARS-CoV-2 infection, and vulnerable to its effects. Major actions may be needed to limit the exposure of many wild primate populations to humans. This is not a straightforward problem to solve, as human proximity to wild primates may also help to keep them safe. A recent special issue of the American Journal of Primatology, and ongoing chronicles by researchers in the International Primatological Society (@IPS_PrimateNews, #IPSCovidChronicals on Twitter) discusses some of the issues and impact around COVID-19 and primatology.

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