Generalism and the evolution of parasite virulence

Leggett, Helen C.; Buckling, Angus; Long, Gráinne H.; Boots, Mike

doi:10.1016/j.tree.2013.07.002

Cited by 139 publications

(162 citation statements)

References 56 publications

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“…By contrast, evidence that the trade-off theory explains the large differences we observe across parasite species in virulence is lacking [12,18,20–22]. One possible explanation for why patterns of virulence across species have been difficult to explain is that mechanistic interactions between hosts and parasites may vary across species and swamp any simple relationship between growth rate and virulence [10,12,18].…”

Section: Introductionmentioning

confidence: 99%

Growth rate, transmission mode and virulence in human pathogens

Leggett

Cornwallis

Buckling

et al. 2017

Phil. Trans. R. Soc. B

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The harm that pathogens cause to hosts during infection, termed virulence, varies across species from negligible to a high likelihood of rapid death. Classic theory for the evolution of virulence is based on a trade-off between pathogen growth, transmission and host survival, which predicts that higher within-host growth causes increased transmission and higher virulence. However, using data from 61 human pathogens, we found the opposite correlation to the expected positive correlation between pathogen growth rate and virulence. We found that (i) slower growing pathogens are significantly more virulent than faster growing pathogens, (ii) inhaled pathogens and pathogens that infect via skin wounds are significantly more virulent than pathogens that are ingested, but (iii) there is no correlation between symptoms of infection that aid transmission (such as diarrhoea and coughing) and virulence. Overall, our results emphasize how virulence can be influenced by mechanistic life-history details, especially transmission mode, that determine how parasites infect and exploit their hosts.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

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Section: Introductionmentioning

confidence: 99%

Growth rate, transmission mode and virulence in human pathogens

Leggett

Cornwallis

Buckling

et al. 2017

Phil. Trans. R. Soc. B

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“…The opportunists with a wide host range have a higher likelihood to find potential hosts than host-specialists [28, 29]. They are therefore more likely to be involved in coinfections.…”

Section: Introductionmentioning

confidence: 99%

Coinfection outcome in an opportunistic pathogen depends on the inter-strain interactions

2017

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BackgroundIn nature, organisms are commonly coinfected by two or more parasite strains, which has been shown to influence disease virulence. Yet, the effects of coinfections of environmental opportunistic pathogens on disease outcome are still poorly known, although as host-generalists they are highly likely to participate in coinfections. We asked whether coinfection with conspecific opportunistic strains leads to changes in virulence, and if these changes are associated with bacterial growth or interference competition. We infected zebra fish (Danio rerio) with three geographically and/or temporally distant environmental opportunist Flavobacterium columnare strains in single and in coinfection. Growth of the strains was studied in single and in co-cultures in liquid medium, and interference competition (growth-inhibiting ability) on agar.ResultsThe individual strains differed in their virulence, growth and ability for interference competition. Number of coinfecting strains significantly influenced the virulence of infection, with three-strain coinfection differing from the two-strain and single infections. Differences in virulence seemed to associate with the identity of the coinfecting bacterial strains, and their pairwise interactions. This indicates that benefits of competitive ability (production of growth-inhibiting compounds) for virulence are highest when multiple strains co-occur, whereas the high virulence in coinfection may be independent from in vitro bacterial growth.ConclusionsIntraspecific competition can lead to plastic increase in virulence, likely caused by faster utilization of host resources stimulated by the competitive interactions between the strains. However, disease outcome depends both on the characteristics of individual strains and their interactions. Our results highlight the importance of strain interactions in disease dynamics in environments where various pathogen genotypes co-occur.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0922-2) contains supplementary material, which is available to authorized users.

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“…The availability of multiple reservoir species may also affect a pathogen’s virulence and mask the fitness effects of pathogen infection in wild hosts (Leggett et al 2013). Moreover, in a multi-host-pathogen system there is potential to underestimate the impact of pathogens, as sentinel species used in lab studies may not be representative if they are assayed under conditions of resource superabundance.…”

Section: Introductionmentioning

confidence: 99%

Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated?

2017

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Slow bee paralysis virus (SBPV)—previously considered an obligate honeybee disease—is now known to be prevalent in bumblebee species. SBPV is highly virulent in honeybees in association with Varroa mites, but has been considered relatively benign otherwise. However, condition-dependent pathogens can appear asymptomatic under good, resource abundant conditions, and negative impacts on host fitness may only become apparent when under stressful or resource-limited conditions. We tested whether SBPV expresses condition-dependent virulence in its bumblebee host, Bombus terrestris, by orally inoculating bees with SBPV and recording longevity under satiated and starvation conditions. SBPV infection resulted in significant virulence under starvation conditions, with infected bees 1.6 times more likely to die at any given time point (a median of 2.3 h earlier than uninfected bees), whereas there was no effect under satiated conditions. This demonstrates clear condition-dependent virulence for SBPV in B. terrestris. Infections that appear asymptomatic in non-stressful laboratory assays may nevertheless have significant impacts under natural conditions in the wild. For multi-host pathogens such as SBPV, the use of sentinel host species in laboratory assays may further lead to the underestimation of pathogen impacts on other species in nature. In this case the impact of ‘honeybee viruses’ on wild pollinators may be underestimated, with detrimental effects on conservation and food security. Our results highlight the importance of multiple assays and multiple host species when testing for virulence, in order for laboratory studies to accurately inform conservation policy and mitigate disease impacts in wild pollinators.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-017-3851-2) contains supplementary material, which is available to authorized users.

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Generalism and the evolution of parasite virulence

Cited by 139 publications

References 56 publications

Growth rate, transmission mode and virulence in human pathogens

Growth rate, transmission mode and virulence in human pathogens

Coinfection outcome in an opportunistic pathogen depends on the inter-strain interactions

Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated?

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