Changes to migration routes and phenology create novel contact patterns among hosts and pathogens. These novel contact patterns can lead to pathogens spilling over between resident and migrant populations. Predicting the consequences of such pathogen spillover events requires understanding how pathogen evolution depends on host movement behaviour. Following spillover, pathogens may evolve changes in their transmission rate and virulence phenotypes because different strategies are favoured by resident and migrant host populations. There is conflict in current theoretical predictions about what those differences might be. Some theory predicts lower pathogen virulence and transmission rates in migrant populations because migrants have lower tolerance to infection. Other theoretical work predicts higher pathogen virulence and transmission rates in migrants because migrants have more contacts with susceptible hosts. We aim to understand how differences in tolerance to infection and host pace of life act together to determine the direction of pathogen evolution following pathogen spillover from a resident to a migrant population. We constructed a spatially implicit model in which we investigate how pathogen strategy changes following the addition of a migrant population. We investigate how differences in tolerance to infection and pace of life between residents and migrants determine the effect of spillover on pathogen evolution and host population size. When the paces of life of the migrant and resident hosts are equal, larger costs of infection in the migrants lead to lower pathogen transmission rate and virulence following spillover. When the tolerance to infection in migrant and resident populations is equal, faster migrant paces of life lead to increased transmission rate and virulence following spillover. However, the opposite can also occur: when the migrant population has lower tolerance to infection, faster migrant paces of life can lead to decreases in transmission rate and virulence. Predicting the outcomes of pathogen spillover requires accounting for both differences in tolerance to infection and pace of life between populations. It is also important to consider how movement patterns of populations affect host contact opportunities for pathogens. These results have implications for wildlife conservation, agriculture and human health.
Novel pathogen introduction triggers rapid evolution in animal social movement strategies
Animal sociality emerges from individual decisions on how to balance the costs and benefits of being sociable. Novel pathogens introduced into wildlife populations should increase the costs of sociality, selecting against gregariousness. Using an individual-based model that captures essential features of pathogen transmission among social hosts, we show how novel pathogen introduction provokes the rapid evolutionary emergence and coexistence of distinct social movement strategies. These strategies differ in how they trade the benefits of social information against the risk of infection. Overall, pathogen-risk-adapted populations move more and have fewer associations with other individuals than their pathogen-risk-naive ancestors, reducing disease spread. Host evolution to be less social can be sufficient to cause a pathogen to be eliminated from a population, which is followed by a rapid recovery in social tendency. Our conceptual model is broadly applicable to a wide range of potential host–pathogen introductions and offers initial predictions for the eco-evolutionary consequences of wildlife pathogen spillover scenarios and a template for the development of theory in the ecology and evolution of animals’ movement decisions.
more » « less- Award ID(s):
- 2211287
- NSF-PAR ID:
- 10509800
- Publisher / Repository:
- eLife
- Date Published:
- Journal Name:
- eLife
- Volume:
- 12
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Barrett, Louise (Ed.)Abstract Direct pathogen and parasite transmission is fundamentally driven by a population’s contact network structure and its demographic composition and is further modulated by pathogen life-history traits. Importantly, populations are most often concurrently exposed to a suite of pathogens, which is rarely investigated, because contact networks are typically inferred from spatial proximity only. Here, we use 5 years of detailed observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) that distinguish between four different types of social contact. We investigate how demography (sex and age) affects these different social behaviors. Three of the four social behaviors can be used as a proxy for understanding key routes of direct pathogen transmission (sexual contact, skin contact, and aerosol contact of respiratory vapor above the water surface). We quantify the demography-dependent network connectedness, representing the risk of exposure associated with the three pathogen transmission routes, and quantify coexposure risks and relate them to individual sociability. Our results suggest demography-driven disease risk in bottlenose dolphins, with males at greater risk than females, and transmission route-dependent implications for different age classes. We hypothesize that male alliance formation and the divergent reproductive strategies in males and females drive the demography-dependent connectedness and, hence, exposure risk to pathogens. Our study provides evidence for the risk of coexposure to pathogens transmitted along different transmission routes and that they relate to individual sociability. Hence, our results highlight the importance of a multibehavioral approach for a more complete understanding of the overall pathogen transmission risk in animal populations, as well as the cumulative costs of sociality.more » « less
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null (Ed.)Anthropogenic landscape modification such as urbanization can expose wildlife to toxicants, with profound behavioural and health effects. Toxicant exposure can alter the local transmission of wildlife diseases by reducing survival or altering immune defence. However, predicting the impacts of pathogens on wildlife across their ranges is complicated by heterogeneity in toxicant exposure across the landscape, especially if toxicants alter wildlife movement from toxicant-contaminated to uncontaminated habitats. We developed a mechanistic model to explore how toxicant effects on host health and movement propensity influence range-wide pathogen transmission, and zoonotic exposure risk, as an increasing fraction of the landscape is toxicant-contaminated. When toxicant-contaminated habitat is scarce on the landscape, costs to movement and survival from toxicant exposure can trap infected animals in contaminated habitat and reduce landscape-level transmission. Increasing the proportion of contaminated habitat causes host population declines from combined effects of toxicants and infection. The onset of host declines precedes an increase in the density of infected hosts in contaminated habitat and thus may serve as an early warning of increasing potential for zoonotic spillover in urbanizing landscapes. These results highlight how sublethal effects of toxicants can determine pathogen impacts on wildlife populations that may not manifest until landscape contamination is widespread.more » « less
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null (Ed.)Abstract The COVID-19 pandemic imposed new norms on human interactions, perhaps best reflected in the widespread application of social distancing. But social distancing is not a human invention and has evolved independently in species as dissimilar as apes and lobsters. Epidemics are common in the wild, where their spread is enhanced by animal movement and sociality while curtailed by population fragmentation, host behavior, and the immune systems of hosts. In the present article, we explore the phenomenon of behavioral immunity in wild animals as compared with humans and its relevance to the control of disease in nature. We start by explaining the evolutionary benefits and risks of sociality, look at how pathogens have shaped animal evolution, and provide examples of pandemics in wild animal populations. Then we review the known occurrences of social distancing in wild animals, the cues used to enforce it, and its efficacy in controlling the spread of diseases in nature.more » « less
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Acute infections can alter foraging and movement behaviors relevant to sociality and pathogen spread. However, few studies have directly examined how acute infections caused by directly transmitted pathogens influence host social preferences. While infected hosts often express sickness behaviors (e.g., lethargy) that can reduce social associations with conspecifics, enhanced sociality during infection might be favored in some systems if social grouping improves host survival of infection. Directly assaying social preferences of infected hosts is needed to elucidate potential changes in social preferences that may act as a form of behavioral tolerance (defined as using behavior to minimize fitness costs of infection). We tested how infection alters sociality in juvenile house finches (more » « less
Haemorhous mexicanus ), which are both highly gregarious and particularly susceptible to infection by the bacterial pathogenMycoplasma gallisepticum (MG). We inoculated 33 wild‐caught but captive‐held juvenile house finches with MG or media (sham control). At peak infection, birds were given a choice assay to assess preference for associating near a flock versus an empty cage. We then repeated this assay after all birds had recovered from infection. Infected birds were significantly more likely than controls to spend time associating with, and specifically foraging near, the flock. However, after infected birds had recovered from MG infection, there were no significant differences in the amount of time birds in each treatment spent with the flock. These results indicate augmented social preferences during active infection, potentially as a form of behavioral tolerance. Notably, infected birds showed strong social preferences regardless of variation in disease severity or pathogen loads, with 14/19 harboring high loads (5–6 log10copies of MG) at the time of the assay. Overall, our results show that infection with a directly transmitted pathogen can augment social preferences, with important implications for MG spread in natural populations.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.81805
