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The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission.

ABSTRACT: BACKGROUND:The freshwater snail Biomphalaria acts as the intermediate host of Schistosoma mansoni, a globally important human parasite. Understanding the population structure of intermediate host species can elucidate transmission dynamics and assist in developing appropriate control methods. METHODS:We examined levels of population genetic structure and diversity in 29 populations of Biomphalaria choanomphala collected around the shoreline of Lake Victoria in Uganda, Kenya and Tanzania, where S. mansoni is hyper-endemic. Molecular markers were utilized to estimate the degree to which snail populations are genetically differentiated from one another. RESULTS:High levels of snail genetic diversity were found coupled with evidence of geographically-determined population structure but low levels of local inbreeding. The data are consistent with an effect of schistosome infection on population structure of intermediate host snails, but other factors, such as habitat and historical demographic changes, could also be important determinants of the degree of population genetic structure in Biomphalaria choanomphala. CONCLUSIONS:The low stratification of populations and high genetic diversity indicates potentially less local compatibility with intermediate snail populations than previously theorized, and highlights the importance of coordinated parasite control strategies across the region.

SUBMITTER: Standley CJ

PROVIDER: S-EPMC4254209 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission.

Standley Claire J CJ Goodacre Sara L SL Wade Christopher M CM Stothard J Russell JR

Parasites & vectors 20141119

<h4>Background</h4>The freshwater snail Biomphalaria acts as the intermediate host of Schistosoma mansoni, a globally important human parasite. Understanding the population structure of intermediate host species can elucidate transmission dynamics and assist in developing appropriate control methods.<h4>Methods</h4>We examined levels of population genetic structure and diversity in 29 populations of Biomphalaria choanomphala collected around the shoreline of Lake Victoria in Uganda, Kenya and Ta ...[more]

PMID: 25406437

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Project description:Glossina fuscipes fuscipes is the primary vector of trypanosomiasis in humans and livestock in Uganda. The Lake Victoria basin has been targeted for tsetse eradication using a rolling carpet initiative, from west to east, with four operational blocks (3 in Uganda and 1 in Kenya), under a Pan-African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC). We screened tsetse flies from the three Ugandan PATTEC blocks for genetic diversity at 15 microsatellite loci from continental and offshore populations to provide empirical data to support this initiative.We collected tsetse samples from 11 sites across the Lake Victoria basin in Uganda. We performed genetic analyses on 409 of the collected tsetse flies and added data collected for 278 individuals in a previous study. The flies were screened across 15 microsatellite loci and the resulting data were used to assess the temporal stability of populations, to analyze patterns of genetic exchange and structuring, to estimate dispersal rates and evaluate the sex bias in dispersal, as well as to estimate demographic parameters (NE and NC).We found that tsetse populations in this region were stable over 4-16 generations and belong to 4 genetic clusters. Two genetic clusters (1 and 2) corresponded approximately to PATTEC blocks 1 and 2, while the other two (3 and 4) fell within PATTEC block 3. Island populations grouped into the same genetic clusters as neighboring mainland sites, suggesting presence of gene flow between these sites. There was no evidence of the stretch of water separating islands from the mainland forming a significant barrier to dispersal. Dispersal rates ranged from 2.5 km per generation in cluster 1 to 14 km per generation in clusters 3 and 4. We found evidence of male-biased dispersal. Few breeders are successfully dispersing over large distances. Effective population size estimates were low (33-310 individuals), while census size estimates ranged from 1200 (cluster 1) to 4100 (clusters 3 and 4). We present here a novel technique that adapts an existing census size estimation method to sampling without replacement, the scheme used in sampling tsetse flies.Our study suggests that different control strategies should be implemented for the three PATTEC blocks and that, given the high potential for re-invasion from island sites, mainland and offshore sites in each block should be targeted at the same time.

Project description:BackgroundSchistosomiasis is a neglected tropical disease endemic in 54 countries. A major Schistosoma species, Schistosoma mansoni, is sustained via a life cycle that includes both human and snail hosts. Mathematical models of S. mansoni transmission, used to elucidate the complexities of the transmission cycle and estimate the impact of intervention efforts, often focus primarily on the human host. However, S. mansoni incurs physiological costs in snails that vary with the age of the snail when first infected. Snail demography and the age of snail infection could thus affect the force of infection experienced by humans, which is frequently used to predict the impact of various control strategies.MethodsTo address how these snail host and parasite interactions influence model predictions, we developed deterministic models of schistosomiasis transmission that include varying complexity in the snail population age structure. Specifically, we examined how model outputs, such as schistosome prevalence in human and snail populations, respond to the inclusion of snail age structure.ResultsOur models suggest that snail population age structure modifies the force of infection experienced by humans and the relationship between snail infection prevalence and corresponding human infection prevalence. There are significant differences in estimated snail infection, cercarial density and mean worm burden between models without snail population dynamics and those with snail populations, and between models with a homogeneous snail population and those with age stratification. The variation between finely age-stratified snail populations and those grouped into only juvenile and adult life stages is, however, minimal.ConclusionsThese results indicate that including snails and snail age structure in a schistosomiasis transmission model alters the relationship between snail and human infection prevalence. This highlights the importance of accounting for a heterogeneous intermediate host population in models of schistosomiasis transmission where the impact of proposed control measures is being considered.

Dataset Information

The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission.

Publications

The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission.

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