Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Rigaud, Thierry; Perrot‐Minnot, Marie‐Jeanne; Brown, Mark J. F.

doi:10.1098/rspb.2010.1163

Cited by 262 publications

(276 citation statements)

References 89 publications

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“…However, parasite gametocytes were observed in some of the blood smears, thus supporting the conclusion that the identified lineages can complete development in the analysed gull species. Co-infections by multiple parasite species are well documented across many animal systems (Rigaud et al 2010;Knowles et al 2013) and we found that a substantial proportion of the gulls were infected with two or more parasites. To what extent parasites in co-infections compete within the host is poorly investigated but it is possible that infections by one parasite may protect the host from other infections.…”

Section: Discussionmentioning

confidence: 73%

High prevalence of Leucocytozoon parasites in fresh water breeding gulls

Zagalska-Neubauer

Bensch

2015

J Ornithol

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Seabirds are regarded as a group of species with relatively low levels or even complete lack of blood parasites. We used PCR to amplify a DNA fragment from the cytochrome b gene of the parasites to search for infections of the genera Plasmodium, Haemoproteus and Leucocytozoon in individuals of two sympatrically breeding gull species, the Herring Gull Larus argentatus, the Caspian Gull Larus cachinnans and their hybrids. Out of 56 analysed individuals, 53 (95 %) were identified as infected with Leucocytozoon, whereas three individuals carried double and triple infections with at least one Leucocytozoon and one Plasmodium lineages. No Haemoproteus lineage was detected. The most common lineage (LARCAC02), for the first time reported here, was found in 51 (96 %) of all infected birds, and 14 gulls carried two Leucocytozoon lineages. We analysed the evolutionary relationship of Leucocytozoon lineages from the Herring and Caspian Gull and other bird species. Our results show that (1) the two identified Leucocytozoon lineages are not closely related as they belong to two distinctly different clusters. Moreover, (2) seabirds breeding inland could be highly infected with blood parasites and (3)

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Section: Discussionmentioning

confidence: 73%

High prevalence of Leucocytozoon parasites in fresh water breeding gulls

Zagalska-Neubauer

Bensch

2015

J Ornithol

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“…While biomedical research has traditionally focused on isolated interactions between a single host and a single parasite, growing evidence indicates that interactions among coinfecting parasites can affect host pathology, parasite transmission, and virulence evolution (33). Our work with a guild of amphibian parasites illustrates the importance of this cryptic component of biodiversity in affecting both parasite infection success and host pathology.…”

Section: Discussionmentioning

confidence: 86%

Parasite diversity and coinfection determine pathogen infection success and host fitness

Johnson

Hoverman

2012

Proc. Natl. Acad. Sci. U.S.A.

156

161

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While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.microbiome | parasite competition | emerging infectious disease | ecosystem function | amphibian decline E cological research has focused increasingly on the importance of changes in biodiversity, thereby forming a fundamental link between community and ecosystem ecology (1-4). The loss or gain of species into a community, often in association with anthropogenic activities, can have remarkable effects on productivity, carbon storage, nutrient cycling, and species invasions (5-8). More recently, this line of inquiry has been extended to explore the role of biodiversity in affecting parasite transmission (i.e., the dilution effect; ref. 9). Building from historical research on agricultural plant communities (10), a series of recent studies has reported an inverse relationship between host diversity and the risk of disease in humans, plants, birds, amphibians, and corals (9). On the basis of experimental manipulations of host diversity, common mechanisms for this relationship involve changes in susceptible host density, such that higher diversity leads to a concomitant decline in susceptible hosts, or in encounter reduction, with added species interfering with parasite transmission (11,12).Des...

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“…a fixed dispersal strategy) [3][4][5]. While this assumption makes transmission models tractable, transmission processes are probably more complex and nuanced than is generally recognized [6]. For directly transmitted symbionts, transmission from one host to another is largely synonymous with the dispersal of free-living organisms from one patch to another, and during host contact each individual symbiont makes a decision to disperse, or to stay with their current host.…”

Section: Introductionmentioning

confidence: 99%

A symbiont's dispersal strategy: condition-dependent dispersal underlies predictable variation in direct transmission among hosts

2015

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Direct horizontal transmission of pathogenic and mutualistic symbionts has profound consequences for host and symbiont fitness alike. While the importance of contact rates for transmission is widely recognized, the processes that underlie variation in transmission during contact are rarely considered. Here, we took a symbiont's perspective of transmission as a form of dispersal and adopted the concept of condition-dependent dispersal strategies from the study of free-living organisms to understand and predict variation in transmission in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. Field study showed that symbiont reproductive success was correlated with host size and competition among worms for microhabitats. Laboratory experiments demonstrated high variability in transmission among host contacts. Moreover, symbionts were more likely to disperse when host size and competition for microhabitat created a fitness environment below a discrete minimum threshold. A predictive model based on a condition-dependent symbiont dispersal strategy correctly predicted transmission in 95% of experimental host encounters and the exact magnitude of transmission in 67%, both significantly better than predictions that assumed a fixed transmission rate. Our work provides a dispersalbased understanding of symbiont transmission and suggests adaptive symbiont dispersal strategies can explain variation in transmission dynamics and complex patterns of host infection.

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Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Cited by 262 publications

References 89 publications

High prevalence of Leucocytozoon parasites in fresh water breeding gulls

High prevalence of Leucocytozoon parasites in fresh water breeding gulls

Parasite diversity and coinfection determine pathogen infection success and host fitness

A symbiont's dispersal strategy: condition-dependent dispersal underlies predictable variation in direct transmission among hosts

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