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1. Sex, synchrony, and skin contact: integrating multiple behaviors to assess pathogen transmission risk

   https://doi.org/10.1093/beheco/araa002  

   Leu, Stephan T ; Sah, Pratha ; Krzyszczyk, Ewa ; Jacoby, Ann-Marie ; Mann, Janet ; Bansal, Shweta ( February 2020 , Behavioral Ecology)

   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. 

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2. Seasonal changes in network connectivity and consequences for pathogen transmission in a solitary carnivore

   https://doi.org/10.1038/s41598-023-44815-y  

   Gilbertson, Marie L. J. ; Hart, S. Niamh ; VanderWaal, Kimberly ; Onorato, Dave ; Cunningham, Mark ; VandeWoude, Sue ; Craft, Meggan E. ( October 2023 , Scientific Reports)

   Seasonal variation in habitat use and animal behavior can alter host contact patterns with potential consequences for pathogen transmission dynamics. The endangered Florida panther (Puma concolor coryi) has experienced significant pathogen-induced mortality and continues to be at risk of future epidemics. Prior research has found increased panther movement in Florida’s dry versus wet seasons, which may affect panther population connectivity and seasonally increase potential pathogen transmission. Our objective was to determine if Florida panthers are more spatially connected in dry seasons relative to wet seasons, and test if identified connectivity differences resulted in divergent predicted epidemic dynamics. We leveraged extensive panther telemetry data to construct seasonal panther home range overlap networks over an 11 year period. We tested for differences in network connectivity, and used observed network characteristics to simulate transmission of a broad range of pathogens through dry and wet season networks. We found that panthers were more spatially connected in dry seasons than wet seasons. Further, these differences resulted in a trend toward larger and longer pathogen outbreaks when epidemics were initiated in the dry season. Our results demonstrate that seasonal variation in behavioral patterns—even among largely solitary species—can have substantial impacts on epidemic dynamics.

    

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3. What Does Tolerance Mean for Animal Disease Dynamics When Pathology Enhances Transmission?

   https://doi.org/10.1093/icb/icz065  

   Henschen, Amberleigh E. ; Adelman, James S. ( May 2019 , Integrative and Comparative Biology)

   Host competence, or how well an individual transmits pathogens, varies substantially within and among animal populations. As this variation can alter the course of epidemics and epizootics, revealing its underlying causes will help predict and control the spread of disease. One host trait that could drive heterogeneity in competence is host tolerance, which minimizes fitness losses during infection without decreasing pathogen load. In many cases, tolerance should increase competence by extending infectious periods and enabling behaviors that facilitate contact among hosts. However, we argue that the links between tolerance and competence are more varied. Specifically, the different physiological and behavioral mechanisms by which hosts achieve tolerance should have a range of effects on competence, enhancing the ability to transmit pathogens in some circumstances and impeding it in others. Because tissue-based pathology (damage) that reduces host fitness is often critical for pathogen transmission, we focus on two mechanisms that can underlie tolerance at the tissue level: damage-avoidance and damage-repair. As damage-avoidance reduces transmission-enhancing pathology, this mechanism is likely to decrease host competence and pathogen transmission. In contrast, damage-repair does not prevent transmission-relevant pathology from occurring. Rather, damage-repair provides new, healthy tissues that pathogens can exploit, likely extending the infectious period and increasing host competence. We explore these concepts through graphical models and present three disease systems in which damage-avoidance and damage-repair alter host competence in the predicted directions. Finally, we suggest that by incorporating these links, future theoretical studies could provide new insights into infectious disease dynamics and host–pathogen coevolution.

    

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4. The dynamics of evolutionary rescue from a novel pathogen threat in a host metapopulation

   https://doi.org/10.1038/s41598-021-90407-z  

   Jiao, Jing ; Fefferman, Nina ( December 2021 , Scientific Reports)

   Abstract When a novel disease strikes a naïve host population, there is evidence that the most immediate response can involve host evolution while the pathogen remains relatively unchanged. When hosts also live in metapopulations, there may be critical differences in the dynamics that emerge from the synergy among evolutionary, ecological, and epidemiological factors. Here we used a Susceptible-Infected-Recovery model to explore how spatial and temporal ecological factors may drive the epidemiological and rapid-evolutionary dynamics of host metapopulations. For simplicity, we assumed two host genotypes: wild type, which has a positive intrinsic growth rate in the absence of disease, and robust type, which is less likely to catch the infection given exposure but has a lower intrinsic growth rate in the absence of infection. We found that the robust-type host would be strongly selected for in the presence of disease when transmission differences between the two types is large. The growth rate of the wild type had dual but opposite effects on host composition: a smaller increase in wild-type growth increased wild-type competition and lead to periodical disease outbreaks over the first generations after pathogen introduction, while larger growth increased disease by providing more susceptibles, which increased robust host density but decreased periodical outbreaks. Increased migration had a similar impact as the increased differential susceptibility, both of which led to an increase in robust hosts and a decrease in periodical outbreaks. Our study provided a comprehensive understanding of the combined effects among migration, disease epidemiology, and host demography on host evolution with an unchanging pathogen. The findings have important implications for wildlife conservation and zoonotic disease control. 

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5. Pathogen evolution following spillover from a resident to a migrant host population depends on interactions between host pace of life and tolerance to infection

   https://doi.org/10.1111/1365-2656.14075  

   Torstenson, Martha ; Shaw, Allison K. ( April 2024 , Journal of Animal Ecology)

   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.

    

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