Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes

White, Lauren A.; Forester, James D.; Craft, Meggan E.

doi:10.1111/oik.04527

Cited by 28 publications

(68 citation statements)

References 69 publications

(86 reference statements)

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“…are the most prevalent multicellular parasites in wild populations [25], transmit directly through contact between hosts [26], and reduce host fitness [9,27,28] in proportion to infection load [10,[28][29][30]. My results highlight the dynamic nature of both behaviour and parasite infection, and the importance of accounting for within-and between-individual variation in predicting disease spread [4,5,22]. and fed daily on flake food and Artemia.…”

Section: Introductionmentioning

confidence: 84%

“…An animal's behaviour is fundamentally linked to the ecology and evolution of its parasites: to fully understand the proximate and ultimate forces driving behavioural evolution, we need to better characterize the role of parasites [1][2][3]. Similarly, in this time of unprecedented infectious disease emergence, it is imperative we improve our understanding of how variation in individual behaviour affects the spread of diseases at the population level [1,[4][5][6].…”

Section: Introductionmentioning

confidence: 99%

“…Positive covariation in β c and β p , however, can lead to rapid epidemic spread. Further empirical tests will help elucidate the conditions under which β c and β p covary, and the factors affecting the sign of this relationship [4,5,22].…”

Section: Introductionmentioning

confidence: 99%

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Parasite-induced plasticity in host social behaviour depends on sex and susceptibility

Stephenson

2019

Biol. Lett.

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Understanding the effects of parasites on host behaviour, of host behaviour on parasite infection, and the reciprocal interactions between these processes is vital to improving our understanding of animal behaviour and disease dynamics. However, behaviour and parasite infection are both highly variable within and between individual hosts, and how this variation affects behaviour–parasite feedbacks is poorly understood. For example, it is unclear how an individual's behaviour before infection might change once it becomes infected, or as the infection progresses, and how these changes depend on the host's parasite susceptibility. Here, using the guppy, Poecilia reticulata , and a directly transmitted ectoparasite, Gyrodactylus turnbulli , I show that parasite-induced behavioural plasticity depends on host sex and susceptibility. Among females, time spent shoaling (sociality), a behaviour that increases parasite transmission, did not depend on infection status (infected/not) or susceptibility. By contrast, male sociality in the absence of infection was negatively correlated with susceptibility, suggesting that the most susceptible males use behaviour to avoid infection. However, in late infection, when parasite transmission is most likely, male sociality and susceptibility became positively correlated, suggesting that susceptible males modify their behaviour upon infection potentially to increase transmission and mating opportunities. I discuss the implications of these patterns for disease dynamics.

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Section: Introductionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

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Parasite-induced plasticity in host social behaviour depends on sex and susceptibility

Stephenson

2019

Biol. Lett.

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“…Second, we assume that social contacts do not covary with pathogen characteristics and remain unaltered after an infection is introduced into a population. Infection has in fact been shown to alter the social connectivity of hosts (Croft et al, 2011;Lopes, Block, & König, 2016) and recent theoretical work has demonstrated that negative correlations between transmissibility and contact rate can diminish the impact of connectivity (White, Forester, & Craft, 2017…”

Section: Discussionmentioning

confidence: 99%

Disease implications of animal social network structure: A synthesis across social systems

Sah

Mann

Bansal

2018

Journal of Animal Ecology

110

137

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The disease costs of sociality have largely been understood through the link between group size and transmission. However, infectious disease spread is driven primarily by the social organization of interactions in a group and not its size. We used statistical models to review the social network organization of 47 species, including mammals, birds, reptiles, fish and insects by categorizing each species into one of three social systems, relatively solitary, gregarious and socially hierarchical. Additionally, using computational experiments of infection spread, we determined the disease costs of each social system. We find that relatively solitary species have large variation in number of social partners, that socially hierarchical species are the least clustered in their interactions, and that social networks of gregarious species tend to be the most fragmented. However, these structural differences are primarily driven by weak connections, which suggest that different social systems have evolved unique strategies to organize weak ties. Our synthetic disease experiments reveal that social network organization can mitigate the disease costs of group living for socially hierarchical species when the pathogen is highly transmissible. In contrast, highly transmissible pathogens cause frequent and prolonged epidemic outbreaks in gregarious species. We evaluate the implications of network organization across social systems despite methodological challenges, and our findings offer new perspective on the debate about the disease costs of group living. Additionally, our study demonstrates the potential of meta-analytic methods in social network analysis to test ecological and evolutionary hypotheses on cooperation, group living, communication and resilience to extrinsic pressures.

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“…A variety of methods, often applied during or after an epidemic, have demonstrated this variation in natural systems [5,6]. However, predicting a priori which forms of heterogeneity will result in individuals who contribute disproportionately more secondary infections than the average infected individual (i.e., superspreaders; see [3] for details) represents a notable challenge in disease ecology [7].…”

Section: Introductionmentioning

confidence: 99%

Using movement data to estimate contact rates in a simulated environmentally-transmitted disease system

Dougherty

et al. 2018

Preprint

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Agent-based models have become important tools in ecology, particularly in the study of infectious disease dynamics. Simulations of near-continuous movement paths guided by empirical data offer new avenues of investigation into disease transmission. Here, we simulate the spatiotemporal transmission dynamics of anthrax, the acute disease caused by the bacterium Bacillus anthracis, a pathogen transmitted primarily via environmental reservoirs. We explore how calculations of the probabilities of contact between a host and infectious reservoirs are affected by the scale and method of analysis. At both the landscape and individual scales, empirical movement tracks offer previously unattainable estimates of impacts of movement decisions on contact rate metrics. However, the analytical method selected for the calculation of the probability of contact has notable impacts on the resulting estimates, with convex polygons virtually canceling out variation, and unions of local convex hulls (LoCoH methods) and space-time prisms reflecting reasonable variation, but differing in the magnitude of their estimates. The explicit consideration of behavioral states along movement pathways also impacts evaluations of exposure risk, though its effects differ across methods of analysis. Ultimately, simulations demonstrate that the incorporation of movement data into pathogen transmission analyses helps clarify the role of movement processes underlying the observed dynamics of infectious disease.

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Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes

Cited by 28 publications

References 69 publications

Parasite-induced plasticity in host social behaviour depends on sex and susceptibility

Parasite-induced plasticity in host social behaviour depends on sex and susceptibility

Disease implications of animal social network structure: A synthesis across social systems

Using movement data to estimate contact rates in a simulated environmentally-transmitted disease system

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