Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

Nørgaard, Louise Solveig; Phillips, Benjamin L.; Hall, Matthew D.

doi:10.1002/evl3.141

Cited by 16 publications

(24 citation statements)

References 69 publications

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“…However, we find little evidence for manipulation to increase the dispersal. Consistent with previous observations of negative effects of infection in this (59) and other systems (36,(60)(61)(62), core parasites reduced host dispersal, whereas infection with front parasites produced levels of dispersal comparable to uninfected Paramecium. Path analysis indicates that virulence is the main direct predictor of host dispersal in our assays.…”

Section: Trait Relationships: Proximate Causes Of Infected Dispersal supporting

confidence: 91%

An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Noergaard

Zilio

Saade

et al. 2020

Preprint

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21Understanding the occurrence and spatial spread of infectious disease is a major challenge to 22 epidemiologists and evolutionary biologists. Current theory predicts the spread of highly 23 exploitative parasites at the front of spreading epidemics. However, many parasites rely on the 24 dispersal of their hosts to spread to new habitats. This may lead to a conflict between local 25 transmission and spatial spread, counteracting selection for highly virulent parasites. Yet, there 26 are no experimental tests of these hypotheses. Here we investigate parasite evolution in an 27 experiment creating conditions in cores and at fronts of spreading host-parasite populations, 28 using the freshwater host Paramecium caudatum and its bacterial parasite Holospora undulata. 29 We find that parasites from experimental range fronts induce higher rates of host dispersal than 30 parasites from the core. This divergence is accompanied by lower levels of virulence and 31 delayed development of infectious stages of front parasites. We validate these experimental 32 results by fitting an epidemiological model to time-series data independently obtained from the 33 experiment. This combined evidence suggests an evolutionary trade-off between host 34 exploitation (virulence) and host-mediated dispersal, resulting in a shift of the investment in 35 horizontal transmission. In conclusion, our results show that different segments of an epidemic 36 wave may be under divergent selection pressures, shaping the evolution of parasite life history. 37 These findings have important implications for our understanding of the interaction between 38 demography and rapid evolutionary change in spreading populations, which is crucial for the 39 management of emerging diseases, biological invasions and other non-equilibrium scenarios.40 41 42 43 2016; Penczykowski et al., 2016). In spatially homogeneous populations, theory often predicts 48 the spread of highly exploitative (i.e., virulent) parasites with a high transmission potential 49 (Andre and Hochberg, 2005). Outbreaks of disease in the wild, however, generally occur in 50 highly dynamic or patchy host populations, such as in metapopulations or in range expanding 51 and invasive species. Since many parasites spread to new habitats via host-mediated dispersal, 52 the evolution of such parasites will now depend not only on the strategies that maximise 53 transmission in response to changes in host demography (Nørgaard et al., 2019a; Penczykowski 54 et al., 2016), but also on a correlated response to the spatial sorting of hosts with different 55 dispersal capacities across a landscape (see (Calcagno et al., 2006; Perkins et al., 2013). 56 However, how the increased mobility of a host during range expansion processes (Phillips et 57 al., 2010) translates into the emergence and spread of infectious disease, remains unclear due 58 to the high complexity of ecological and evolutionary dynamics at play (see (Dunn and 59 Hatcher , 2015; Perkins et al., 2008; Torchin et al., 2003). 60By explori...

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Section: Trait Relationships: Proximate Causes Of Infected Dispersal supporting

confidence: 91%

An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Noergaard

Zilio

Saade

et al. 2020

Preprint

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“…Interestingly, empirical studies often show the opposite pattern ( S -bias; Cameron et al, 1993; Bradley and Altizer, 2005; Nørgaard et al, 2019), which may be explained by infections weakening hosts and thereby reducing their dispersal capacity. Alternatively, Iritani and Iwasa (2014) show that S -bias may evolve under specific conditions such as strong virulence affecting competitive ability, high rates of parasite release during dispersal, or low virulence for infected emigrants.…”

Section: Resultsmentioning

confidence: 99%

Host-parasite dynamics set the ecological theatre for the evolution of state- and context-dependent dispersal in hosts

Deshpande

Kaltz

Fronhofer

2020

Preprint

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While host-parasite interactions are ubiquitous, the large scale consequences of parasite infections are mainly driven by the spatial context. One trait of pivotal importance for the eco-evolutionary dynamics of such metapopulations is the spatial behaviour of hosts, that is, their dispersal. It is well established that dispersal is not a random process, rather dispersal is informed and may depend on internal and external factors. In host-parasite metapopulations, dispersal may be a function of a host’s infection state, but also of the local context, such as host density or parasite prevalence. Using a dynamical host-parasite metapopulation model, we explore whether host dispersal evolves to be state- and context-dependent and what shapes the evolutionarily stable dispersal reaction norms have. We show that state-dependent dispersal readily evolves in the sense that hosts disperse more when infected. This dispersal bias evolves due to kin selection which is consistent with previous studies. Most importantly, we show that prevalence-dependent dispersal evolves, especially when virulence is high and epidemiological dynamics have predictable signatures. The observed evolutionary outcome, a negatively prevalence-dependent dispersal reaction norm for susceptible hosts, seems counter-intuitive at first. However, our results can be readily explained by the emergent epidemiological dynamics, especially their spatial and temporal correlation patterns. Finally, we show that context-dependency in dispersal may rely on both, prevalence, but also host density cues. Our work provides new insights into the evolution of complex dispersal phenotypes in host-parasite metapopulations as well as on associated feedbacks between ecological dynamics and evolutionary change.

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“…P. ramosa is horizontally transmitted and infection causes severe loss of fecundity, an increase in body size (gigantism) and reduced survival (Clerc et al., 2015; Hall et al., 2019). Both host life history and pathogen performance are influenced by host density and resource intake, with host fecundity and pathogen spore production reduced when food is limited or densities are high (Pulkkinen & Ebert, 2004; Cressler et al., 2014; Nørgaard et al., 2019; although responses can be genotype specific, see Michel et al., 2016). In this study, we used the host genotype HU‐HO‐2 originating from Hungary, and two novel P. ramosa genotypes from Russia (C1) and Germany (C19).…”

Section: Methodsmentioning

confidence: 99%

“…Many host traits, such as filter‐feeding, growth, fecundity, and metabolic rate, often decline with population density, both as a response to reduced food availability, as well as due to conspecific chemical cues or physical crowding (Ban et al., 2008; Burns, 2000; Delong et al., 2014; Michel et al., 2016). These processes in turn reduce the capacity of P. ramosa to proliferate by limiting the resource acquisition and growth of its infected carrier (Clerc et al., 2015; Nørgaard et al., 2019; Pulkkinen & Ebert, 2004). Both host and pathogen performance, therefore, are predicted to be influenced by the scaling relationship of energy intake and expenditure with population density.…”

Section: Introductionmentioning

confidence: 99%

Energetic scaling across different host densities and its consequences for pathogen proliferation

et al. 2020

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The spread of infectious disease is determined by the ability of a pathogen to proliferate within and spread between susceptible hosts. Processes that limit the performance of a pathogen thus occur at two scales: varying with both the availability of energy within a host, and the number of susceptible hosts in a patch. When the rate at which a host intakes and expends energy is density‐dependent, these two processes are intimately linked. By modifying how hosts compete for and expend resources, a shift in population density may contribute to differences in the flow of energy in a host–pathogen system, both in terms of the energy available for a host to grow, reproduce and fight infection, as well as the energy available for a pathogen to exploit. Energy flux, therefore, connects the two contrasting scales of within‐ and between‐host dynamics by directly linking the proliferation of a pathogen to the number of hosts circulating within a patch. We use the host Daphnia magna to explore the relationship between energy intake and expenditure at various population densities, as estimated by feeding and metabolic rates respectively. By infecting hosts with the bacterial pathogen Pasteuria ramosa, we then explore how infection changes the relative balance of energy intake and expenditure, and how this energy scope translates into production of transmission spores. Our work demonstrates that energy intake declines at a faster rate with density than does metabolic rate, leaving more excess energy (i.e. discretionary energy) available for both hosts and their dependent pathogens at low population densities. This energetic advantage translates positively into host and pathogen growth, with the production of mature transmission spores benefiting most from correlated changes in host body size, as well as a direct connection between energy scope and spore loads. Our findings reinforce how patch quality for a pathogen operates at two contrasting scales, with the within‐host proliferation of a pathogen being optimised in energy rich, low density host populations and opportunities for between‐host transmission likely maximised in dense populations. A free Plain Language Summary can be found within the Supporting Information of this article.

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Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

Cited by 16 publications

References 69 publications

An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Host-parasite dynamics set the ecological theatre for the evolution of state- and context-dependent dispersal in hosts

Energetic scaling across different host densities and its consequences for pathogen proliferation

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