Review

Infectious diseases and social distancing in nature

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Science  05 Mar 2021:
Vol. 371, Issue 6533, eabc8881
DOI: 10.1126/science.abc8881

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Nature's “responsible” response to disease

With the emergence of the COVID-19 pandemic, there have been global calls for the implementation of “social distancing” to control transmission. Throughout the world, some have resisted this requirement with the unfounded argument that it is unnecessary or ineffective. Social distancing, however, is a natural consequence of disease across animals, both human and nonhuman. Stockmaier et al. reviewed responses to disease across animal taxa and reveal how these responses naturally limit disease transmission. Understanding such natural responses and their impacts on pathogenic transmission provides epidemiological insight into our own responses to pandemic challenges.

Science, this issue p. eabc8881

Structured Abstract

BACKGROUND

Contagious pathogens can trigger diverse changes in host social behaviors, rewiring their social networks and profoundly influencing the extent and pace of pathogen spread. Although “social distancing” is now an all too familiar strategy to manage COVID-19, nonhuman animals also exhibit a suite of pathogen-induced changes in social interactions, either as precautionary measures by healthy hosts or as physiological consequences of infection in sick individuals. These diverse changes in the social behaviors of both healthy and infected hosts in response to pathogens are widespread across taxa, but we still have much to learn about their underlying mechanisms and epidemiological and evolutionary consequences. Studies of social distancing behaviors in nonhuman animals have the potential to provide important and unique insights into ecological and evolutionary processes relevant to human public health, including pathogen transmission dynamics and virulence evolution.

ADVANCES

We synthesize the literature on pathogen-induced changes in sociality in nonhuman animals and in humans. These include active and passive changes in pathogen-exposed and -unexposed group members occurring both before and after individuals develop an active infection. Behavioral changes that reduce social interactions—and thus pathogen spread—include changes driven by infectious hosts, such as sickness behaviors and active self-isolation, as well as changes driven by healthy hosts, including active avoidance or exclusion of infectious individuals and proactive social distancing in the face of pathogenic threats. Although species have evolved behavioral social distancing because it reduces infection risk, these behaviors also incur costs by limiting access to the many benefits of group living, such as protection against predators and cooperative food finding. Thus, many species appear to have evolved the ability to alter the expression of these behaviors in ways that maximize benefits and minimize costs. The most susceptible individuals of some species show the strongest avoidance of sick conspecifics, and social distancing behaviors are sometimes foregone in interactions with close relatives. Pathogen-induced changes in sociality also apply important selection pressures on pathogens. Because social distancing reduces transmission and thus fitness, pathogens may evolve lower levels of virulence, presymptomatic transmission, or the ability to disguise cues that enable hosts to recognize their presence. Finally, pathogen infection can also increase social interactions when healthy individuals lend aid to pathogen-contaminated or sick conspecifics. Helping sick individuals is a major part of human and eusocial insect societies but is less commonly observed in other, nonhuman animals. Whether pathogens can evolve to elicit helping behavior in hosts, thus augmenting their own transmission, remains unknown.

OUTLOOK

The structure and dynamics of social contact networks fundamentally determine the fate of disease outbreaks, that is, how fast and far they spread and who will be infected. In the race to combat the COVID-19 pandemic, numerous studies have begun to address the public health utility of unprecedented social distancing efforts. Nonhuman animal systems, particularly those with social structures similar to those of humans, present unique opportunities to inform relevant public health questions such as the effectiveness, variability, and required duration of social distancing measures. Further, the experimental tractability of nonhuman animal systems allows study of the coevolutionary dynamics generated by social distancing behaviors, which themselves have public health implications. Selection for or against social distancing behaviors has the potential to create a conflict of interest and could incentivize selfish behaviors that are not in the best interest of everyone.

Social distancing in humans and nonhuman animals.

(A) Pathogen-exposed forager ants self-isolate and their nestmates increase social distance to each other (image: Timothée Brütsch). (B) People social distance during COVID-19 (image: Forest Simon). (C) Sick vampire bats reduce grooming non-close kin (image: Gerald Carter). (D and E) Under certain conditions, Trinidadian guppies avoid parasitized individuals (D), (image: Sean Earnshaw, University of St. Andrews) and house finches avoid sick conspecifics (E) (image: Jeremy Stanley).

Abstract

Spread of contagious pathogens critically depends on the number and types of contacts between infectious and susceptible hosts. Changes in social behavior by susceptible, exposed, or sick individuals thus have far-reaching downstream consequences for infectious disease spread. Although “social distancing” is now an all too familiar strategy for managing COVID-19, nonhuman animals also exhibit pathogen-induced changes in social interactions. Here, we synthesize the effects of infectious pathogens on social interactions in animals (including humans), review what is known about underlying mechanisms, and consider implications for evolution and epidemiology.

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