Predator–spreaders: Predation can enhance parasite success in a planktonic host–parasite system

Cáceres, Carla E.; Knight, Christine J.; Hall, Spencer R.

doi:10.1890/08-2154.1

Cited by 70 publications

(73 citation statements)

References 44 publications

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“…In this context, it has already been shown that accelerated host death is ecologically and epidemiological important. Predation on infected animals, for example, has been shown to be a modifier of infection dynamics in Daphnia [29,30], as predators shortened the infection period by releasing spores from their infected prey during feeding ('sloppy predator' [31]), thereby selecting for accelerated parasite development [30]. Indeed, Pasteuria spores are infectious as early as 14 days post-infection ( [32]; M. Clerc 2012, personal observation) and any extrinsic mortality from this moment onwards would allow transmission and alter evolutionary dynamics.…”

Section: Discussionmentioning

confidence: 99%

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

2015

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How infectious disease agents interact with their host changes during the course of infection and can alter the expression of disease-related traits. Yet by measuring parasite life-history traits at one or few moments during infection, studies have overlooked the impact of variable parasite growth trajectories on disease evolution. Here we show that infection-age-specific estimates of host and parasite fitness components can reveal new insight into the evolution of parasites. We do so by characterizing the within-host dynamics over an entire infection period for five genotypes of the castrating bacterial parasite Pasteuria ramosa infecting the crustacean Daphnia magna. Our results reveal that genetic variation for parasite-induced gigantism, host castration and parasite spore loads increases with the age of infection. Driving these patterns appears to be variation in how well the parasite maintains control of host reproduction late in the infection process. We discuss the evolutionary consequences of this finding with regard to natural selection acting on different ages of infection and the mechanism underlying the maintenance of castration efficiency. Our results highlight how elucidating within-host dynamics can shed light on the selective forces that shape infection strategies and the evolution of virulence.

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Section: Discussionmentioning

confidence: 99%

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

2015

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“…DVM can be highly responsive to climate-driven changes in aquatic ecosystems (De Stasio et al 1993;Kimmel et al 2009;Pierson et al 2009). Other consequences of these changes in vertical habitat gradients and their subsequent effects on DVM include alteration of the overlap between predators and their prey (Williamson and Stoeckel 1990), parasite-host dynamics and rates of parasitism (Caceres et al 2009), and DVM-mediated vertical biogeochemical fluxes .…”

Section: Discussionmentioning

confidence: 99%

Toward a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm

Williamson

Fischer

Bollens

et al. 2011

Limnology & Oceanography

187

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The current prevailing theory of diel vertical migration (DVM) of zooplankton is focused largely on two biotic drivers: food and predation. Yet recent evidence suggests that abiotic drivers such as damaging ultraviolet (UV) radiation and temperature are also important. Here we integrate current knowledge on the effects of abiotic factors on DVM with the current biologically based paradigm to develop a more comprehensive framework for understanding DVM in zooplankton. We focus on ''normal'' (down during the day, up at night) DVM of holoplanktonic, primarily herbivorous zooplankton. This new transparency-regulator hypothesis differentiates between structural drivers, such as temperature and food, that vary little over a 24-h period and dynamic drivers, such as damaging UV radiation and visual predation, that show strong variation over a 24-h period. This hypothesis emphasizes the central role of water transparency in regulating these major drivers of DVM. In less transparent systems, temperature and food are often optimal in the surface waters, visual predators are abundant, and UV radiation levels are low. In contrast, in more transparent systems, vertical thermal gradients tend to be more gradual, food quality and quantity are higher in deeper waters, and visual predator abundance is often lower and damaging UV radiation higher in the surface waters. This transparency-regulator hypothesis provides a more versatile theoretical framework to explain variation in DVM across waters of differing transparency. This hypothesis also enables clearer predictions of how the wide range of ongoing transparency-altering local, regional, and global environmental changes can be expected to influence DVM patterns in both inland and oceanic waters of the world.Diel vertical migrations (DVM) of zooplankton in the world's lakes and oceans comprise some of the most widespread and massive migrations of animals on Earth. These striking migrations across strong vertical habitat gradients have inspired numerous ecological and evolutionary studies addressing mechanisms of habitat selection and consequences for species interactions. These migrations also have important implications for water quality and fisheries production as well as biogeochemical cycling. Natural and anthropogenic environmental changes, such as shifting local land use patterns and regional to global climate change, are altering water transparency and have the potential to affect DVM in lakes and oceans worldwide. The purpose of this article is to provide a common theoretical framework for understanding variation in the drivers of DVM across transparency gradients with a particular emphasis on recent advances in our understanding of the role of ultraviolet radiation (UV).Many environmental factors are recognized as providing both important proximate cues as well as ultimate consequences of adaptive significance for DVM, including light, temperature, food availability, and predation pressures (Table 1; Lampert 1989;Ringelberg 1993;Hays 2003). In spite of the wides...

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“…The two indirect pathways involve nonhost species that we mechanistically connected to yeast epidemics in previous work (Cá ceres et al 2009;Hall et al 2009aHall et al , 2010. Here, we link these species to large-scale habitat structure.…”

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confidence: 95%

Habitat structure and ecological drivers of disease

Penczykowski

Hall

Civitello

et al. 2014

Limnology & Oceanography

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Habitat can influence disease directly, through effects on hosts and parasites, or indirectly, through effects on ecological drivers of disease. We illustrated direct and indirect connections between habitat and outbreaks using a case study in the plankton. We sampled yeast epidemics in 18 populations of the lake zooplankter Daphnia dentifera. Lake size drove variation in two types of habitat structure, size of predation refuges and strength of stratification. Those habitat factors, in turn, indirectly linked to epidemics through two pathways involving nonhost species. In the first pathway, larger lakes had larger hypolimnetic refuges from vertebrate predation and greater densities of Daphnia pulicaria, a completely resistant species that can reduce disease risk for D. dentifera hosts by removing parasite spores from the environment. In lakes with more D. pulicaria, epidemics started later in autumn and remained smaller. In the second pathway, smaller lakes had shallower penetration of light, which correlated with stronger thermal stratification and higher densities of an invertebrate predator (Chaoborus) that spreads disease by releasing spores from infected hosts. Lakes with weaker stratification had fewer of these predators and smaller epidemics. In the second pathway, deeper light penetration may also decrease disease by imposing direct mortality on spores. Thus, this case study shows how habitat structure could influence epidemics through direct and indirect effects on the host-parasite system. Understanding these multiple mechanisms can enhance prediction of disease outbreaks as habitat modification continues in lakes and other ecosystems worldwide.

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Predator–spreaders: Predation can enhance parasite success in a planktonic host–parasite system

Cited by 70 publications

References 44 publications

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

Toward a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm

Habitat structure and ecological drivers of disease

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