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Predicting the effects of parasite co-infection across species boundaries.

ABSTRACT: It is normal for hosts to be co-infected by parasites. Interactions among co-infecting species can have profound consequences, including changing parasite transmission dynamics, altering disease severity and confounding attempts at parasite control. Despite the importance of co-infection, there is currently no way to predict how different parasite species may interact with one another, nor the consequences of those interactions. Here, we demonstrate a method that enables such prediction by identifying two nematode parasite groups based on taxonomy and characteristics of the parasitological niche. From an understanding of the interactions between the two defined groups in one host system (wild rabbits), we predict how two different nematode species, from the same defined groups, will interact in co-infections in a different host system (sheep), and then we test this experimentally. We show that, as predicted, in co-infections, the blood-feeding nematode Haemonchus contortus suppresses aspects of the sheep immune response, thereby facilitating the establishment and/or survival of the nematode Trichostrongylus colubriformis; and that the T. colubriformis-induced immune response negatively affects H. contortus This work is, to our knowledge, the first to use empirical data from one host system to successfully predict the specific outcome of a different co-infection in a second host species. The study therefore takes the first step in defining a practical framework for predicting interspecific parasite interactions in other animal systems.

SUBMITTER: Lello J

PROVIDER: S-EPMC5879626 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Predicting the effects of parasite co-infection across species boundaries.

Lello Joanne J McClure Susan J SJ Tyrrell Kerri K Viney Mark E ME

Proceedings. Biological sciences 20180301 1874

It is normal for hosts to be co-infected by parasites. Interactions among co-infecting species can have profound consequences, including changing parasite transmission dynamics, altering disease severity and confounding attempts at parasite control. Despite the importance of co-infection, there is currently no way to predict how different parasite species may interact with one another, nor the consequences of those interactions. Here, we demonstrate a method that enables such prediction by ident ...[more]

PMID: 29540516

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Project description:Co-infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co-infections may affect their competitive interactions, thereby influencing the success of the parasites and their impact on the host. This may have important consequence for epidemiological and eco-evolutionary dynamics. We examined in two ecological conditions the effect of sequential co-infection on the outcome of infection by two microsporidians, Vavraia culicis and Edhazardia aedis, that infect the mosquito Aedes aegypti. The two parasites have different transmission strategies: V. culicis is transmitted horizontally either among larvae or from adults to larvae, while E. aedis can be transmitted horizontally among larvae or vertically from females to their eggs. We investigated how the timing and order of the co-infection and how the host's food availability affected the parasite's transmission potential (the percentage of individuals that harboured transmissible spores) and the host's juvenile survival, its age at emergence and its longevity. The outcome of co-infection was strongly affected by the order at which the parasites arrived. In co-infections, V. culicis had greater horizontal transmission if it arrived early, whereas the transmission potential of E. aedis, either vertical or horizontal, was not affected by the competitor V. culicis. The availability of food determined the duration of infection leading to variation in mortality and in the transmission potential. For both parasites low food decreased juvenile survival, delayed emergence to adulthood and increased horizontal transmission potential. High food increased juvenile survival and the probability of emergence with higher vertical transmission for E. aedis. Overall, our results suggest that early infection favours transmission and that (a) V. culicis plastically responded to co-infection, (b) E. aedis was not affected by co-infection but it was more susceptible to factors extending or decreasing the time it spent in the host (time of infection and food). Our results emphasize the complexity of the impact of co-infection on host-parasite interactions. In particular, the timing and order of sequential co-infections can result in different within-host dynamics and modify infection outcomes.

Project description:BackgroundCo-infection of the four major species of human malaria parasite Plasmodium falciparum (Pf), P. vivax (Pv), P. malariae (Pm), and P. ovale sp. (Po) is regularly observed, but there is limited understanding of between-species interactions. In particular, little is known about the effects of multiple Plasmodium species co-infections on gametocyte production.MethodsWe developed molecular assays for detecting asexual and gametocyte stages of Pf, Pv, Pm, and Po. This is the first description of molecular diagnostics for Pm and Po gametocytes. These assays were implemented in a unique epidemiological setting in Papua New Guinea with sympatric transmission of all four Plasmodium species permitting a comprehensive investigation of species interactions.FindingsThe observed frequency of Pf-Pv co-infection for asexual parasites (14.7%) was higher than expected from individual prevalence rates (23.8%Pf x 47.4%Pv = 11.3%). The observed frequency of co-infection with Pf and Pv gametocytes (4.6%) was higher than expected from individual prevalence rates (13.1%Pf x 28.2%Pv = 3.7%). The excess risk of co-infection was 1.38 (95% confidence interval (CI): 1.09, 1.67) for all parasites and 1.37 (95% CI: 0.95, 1.79) for gametocytes. This excess co-infection risk was partially attributable to malaria infections clustering in some villages. Pf-Pv-Pm triple infections were four times more frequent than expected by chance alone, which could not be fully explained by infections clustering in highly exposed individuals. The effect of co-infection on parasite density was analyzed by systematic comparison of all pairwise interactions. This revealed a significant 6.57-fold increase of Pm density when co-infected with Pf. Pm gametocytemia also increased with Pf co-infection.ConclusionsHeterogeneity in exposure to mosquitoes is a key epidemiological driver of Plasmodium co-infection. Among the four co-circulating parasites, Pm benefitted most from co-infection with other species. Beyond this, no general prevailing pattern of suppression or facilitation was identified in pairwise analysis of gametocytemia and parasitemia of the four species.Trial registrationThis trial is registered with ClinicalTrials.gov, Trial ID: NCT02143934.

Project description:Species colonizations (both natural and anthropogenic) can be associated with genetic founder effects, where founding populations demonstrate significant genetic bottlenecks compared to native populations. Yet, many successfully established free-living species exhibit little reduction in genetic diversity-possibly due to multiple founding events and/or high propagule pressure during introductions. Less clear, however, is whether parasites may show differential signatures to their free-living hosts. Parasites with indirect life cycles may particularly be more prone to founder effects (i.e., more genetically depauperate) because of inherently smaller founding populations and complex life cycles. We investigated this question in native (east coast) and introduced (west coast) North American populations of a host snail Tritia obsoleta (formerly Ilyanassa obsoleta, the eastern mudsnail) and four trematode parasite species that obligately infect it. We examined genetic diversity, gene flow, and population structure using two molecular markers (mitochondrial and nuclear) for the host and the parasites. In the host snail, we found little to no evidence of genetic founder effects, while the trematode parasites showed significantly lower genetic diversity in the introduced versus native ranges. Moreover, the parasite's final host influenced infection prevalence and genetic diversity: Trematode species that utilized fish as final hosts demonstrated lower parasite diversity and heightened founder effects in the introduced range than those trematodes using birds as final hosts. In addition, inter-regional gene flow was strongest for comparisons that included the putative historical source region (mid-Atlantic populations of the US east coast). Overall, our results broaden understanding of the role that colonization events (including recent anthropogenic introductions) have on genetic diversity in non-native organisms by also evaluating less studied groups like parasites.

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Predicting the effects of parasite co-infection across species boundaries.

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Predicting the effects of parasite co-infection across species boundaries.

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