Animals, like humans, have evolved mechanisms to avoid disease, focusing on the emotion of disgust. An international team of scientists, including Cécile Sarabian and Andrew MacIntosh from Kyoto University, has developed a framework to study disease avoidance behaviors across various species. Over 30 species have been observed using disease avoidance strategies, with predictions for seven additional species. These behaviors are influenced by each species’ ecological niche, sensory environment, and social system.
Could you elaborate more on how the concept of disgust as a protective mechanism operates in the animal kingdom, especially in relation to disease avoidance?
Cécile Sarabian: Disgust can be seen as a protective shield against infections. It is supposed to have evolved to detect sensory cues associated with disease risk (odors, visuals, textures…) and elicit cognitive, physiological and behavioral responses to prevent pathogen, parasite and toxin acquisition. For instance, if we take the facial expression of disgust that humans, macaques and mice exhibit, it prevents the physical entry of disease threats by wrinkling the nose, narrowing the eyes and turning down the corners of the mouth. In the wild, disgust could translate by detecting contaminants such as bodily fluids in the environment, activating one’s physiological immune system and avoiding food or mates associated with these (pending the food or mates are not that attractive!).
Andrew MacIntosh: If we step back a little bit we might ask what the point of an emotion is, and a general answer could be to attune us to behaving in an appropriate way. Fear is a classic example. Its value is that it puts us on alert and prepares us to avoid or escape from danger, for example a predator if you are a prey species going about your everyday business. Fear might stop a subterranean rodent from casually venturing out of its burrow, urging it instead to remain vigilant and tread cautiously. Well, in the same way, disgust might prime an animal to avoid foraging in areas contaminated with feces from its own species, because that constitutes a risk of acquiring a parasite or pathogen, many of which are spread through biological materials such as feces. Or, if you are a female olive baboon, you might hesitate to mate with a male that’s showing genital skin ulcers caused by the bacterial pathogen Treponema pallidum. https://www.science.org/doi/full/10.1126/sciadv.aaw9724
Your research mentions over 30 species exhibiting disease avoidance strategies. Could you provide some specific examples of these behaviors?
CS: Right, in the wild and given the current state-of-the art in research. There would be more if we add to this species tested/observed in other conditions, such as in the lab. One of my favorite illustrations of avoidance behavior comes from western lowland gorillas, with females more susceptible to leaving the group if the alpha male or other members show severe skin lesions on their face, caused by a bacterium called Treponema pallidum. https://doi.org/10.1002/ecy.2786
AM: My afvorite example remains the story of the spiny lobsters infected by the lethal viral pathogen PaV1 that avoid denning with infected conspecifics. Somehow, these lobsters evolved the capacity to perceive when others are infected, and the behavioral mechanism to avoid being inproximity to them, which obviously helps them avoid getting infected in the process. https://www.nature.com/articles/441421a
You’ve identified seven species that were previously overlooked in terms of their disease avoidance strategies. Can you tell us more about these species and what led your team to them?
CS: These species have features representative of different taxa, in terms of sociality, lifestyle, sensory perception, and habitat. We wanted to give an overview of what “disease challenges” could mean for an octopus, a slow loris or a penguin, and how they would cope with these. Members of the team were experts of these species. In the example of slow lorises – these small solitary nocturnal and arboreal primates threatened with extinction – very little is known about how they cope with disease risk. Does their solitary and arboreal lifestyle predispose them to avoid conspecific feces? As habitat fragmentation makes them use the ground more often, would they be ready to avoid such contaminants and terrestrial predators? Could risk perception be used to prepare or select individuals for rehabilitation? These are all fascinating questions that remain to be answered.
AM: One interesting point about colony forming animals like penguins is that they don’t have particularly strong bonds with other individuals in the colony, apart from their mates, yet they require the colony for their survival. I’ve seen Adelie and Emperor penguin colonies on Antarctica, and some of the former are absolutely massive. So space is a limiting factor, and the nests are spaced just far enough apart to allow peace – for the most part – but close enough to allow exchange of biological material like guano! So, nest site selection is a really important part of successful breeding for an Adelie penguin male, and we wonder to what extent contamination from the waste of other penguins plays a role here.
It is also worth noting that emperor penguin colonies can be located from space (satellites) after they’ve already left, based on the huge amounts of guano left behind. So we wonder whether the demands of breeding in such a harsh environment outweigh the costs of contamination, and how individual avoidance behavior might play out under such constrained conditions.
You mentioned that the social systems and ecological niches of species play a crucial role in the development and application of disgust behavior. How does this factor vary across different species and habitats?
CS: A given social trait and habitat would affect exposure to disease and thus risk perception. This would translate by having evolved and/or developed adapted strategies to their way of life. We know, for example, that arboreal primates do not avoid soil-contaminated food as terrestrial primates do. Similarly, solitary aquatic species with a short lifespan such as octopuses may not invest in disease avoidance strategies the same way as long-lived group-living and terrestrial species do. For instance octopuses, like other cephalopods, may detoxify heavy metals they commonly get exposed to in their digestive gland.
AM: the example of the emperor penguin colony I gave above could be another example of animals being contrained to behave in a certain way that reduces their ability to express avoidance behavior. They require each others’ body heat and wind protection to outlast the Antarctic winter. But then again, parasites seem to be less common in Antarctic penguins, unsurprisingly gievn the harsh environmental conditions, and probably especially so in emperor penguins during the Austral winter, so maybe the risks are lower anyway and require less in terms of behavioral avoidance.
Considering species that live in colonies, such as rabbits and penguins, how does community immunity work and how does it affect their response to disease?
CS: Species living in high numbers may use what is called a “dilution effect” to diminish the outcomes of disease spread. Rabbits, for instance, living in high numbers in burrows do not (cannot) avoid each other when a hyper contagious disease outbreak occurs. Instead, they increase contact rate to get exposed to the pathogen before the disease becomes too infectious. Their immune system then becomes competent to recognize the pathogen in the next round. That way, they stay one step ahead of the disease. https://doi.org/10.1136/vr.150.25.776
AM: The classic examples come from eusocial insects like ants. These animals can detect when individuals are infected, and if those affected don’t already self-isolate, then there are others in the colony responsible for blocking them off from the colony or removing them once they succumb to the infection. One of the most classic behaviors related to social immunity – though it started simpler as a means of removing parasites from oneself or otherwise keeping the self clean – is grooming. Our local Japanese macaques spend hours each day doing this, and it seems to be an effective way of keeping louse infestations down. https://www.nature.com/articles/srep22095 see also: https://www.nytimes.com/2016/03/28/science/japanese-monkeys-like-to-socialize-even-with-nits-to-pick.html
How do the behaviors and strategies of animals in avoiding diseases inform our understanding and handling of human health crises, such as the Covid-19 pandemic?
CS: It’s important to know where our behaviors come from. We aren’t the only ones with disease handling strategies. In fact, all animals have to invest in some. Avoidance, the most preventive strategy, can have direct consequences on disease outbreaks if considered. For instance, early epidemiological models of Covid-19 omitted to take into account social distancing, but once considered, the number of cases flattened much earlier.
AM: We wrote about this recently in a paper published in Trends in Ecology and Evolution: https://www.cell.com/trends/ecology-evolution/fulltext/S0169-5347(20)30184-1. One clear outcome of COVID-19 is that it forced us all to think deeply about how we’re all connected, how we’re embedded in this vast social network. Social distancing was our attempt to sever that network, or at least reduce its power to facilitate the spread of the virus. Well, social animals are also embedded in social networks, often at much smaller scales but still with the capacity to put group members at risk of infection. How those networks respond, meaning how individuals change their social behavior in the face of new threats like an emerging disease, gives us a clue into how flexible different species might be. So, learning about disease spread in animal networks, and what behaviors they might deploy to mitigate that spread or alter those networks, might give us some ideas as well about how to structure our own societies in ways that can minimize the risk without severing all ties ubiquitously.
IMAGE CREDIT: Alfonsopazphoto.
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