Genetic Evidence of Contemporary Dispersal of the Intermediate Snail Host of Schistosoma japonicum: Movement of an NTD Host Is Facilitated by Land Use and Landscape Connectivity

PLoS Negl Trop Dis. 2016 Dec 15;10(12):e0005151. doi: 10.1371/journal.pntd.0005151. eCollection 2016 Dec.

Abstract

Background: While the dispersal of hosts and vectors-through active or passive movement-is known to facilitate the spread and re-emergence of certain infectious diseases, little is known about the movement ecology of Oncomelania spp., intermediate snail host of the parasite Schistosoma japonicum, and its consequences for the spread of schistosomiasis in East and Southeast Asia. In China, despite intense control programs aimed at preventing schistosomiasis transmission, there is evidence in recent years of re-emergence and persistence of infection in some areas, as well as an increase in the spatial extent of the snail host. A quantitative understanding of the dispersal characteristics of the intermediate host can provide new insights into the spatial dynamics of transmission, and can assist public health officials in limiting the geographic spread of infection.

Methodology/principal findings: Oncomelania hupensis robertsoni snails (n = 833) were sampled from 29 sites in Sichuan, China, genotyped, and analyzed using Bayesian assignment to estimate the rate of recent snail migration across sites. Landscape connectivity between each site pair was estimated using the geographic distance distributions derived from nine environmental models: Euclidean, topography, incline, wetness, land use, watershed, stream use, streams and channels, and stream velocity. Among sites, 14.4% to 32.8% of sampled snails were identified as recent migrants, with 20 sites comprising >20% migrants. Migration rates were generally low between sites, but at 8 sites, over 10% of the overall host population originated from one proximal site. Greater landscape connectivity was significantly associated with increased odds of migration, with the minimum path distance (as opposed to median or first quartile) emerging as the strongest predictor across all environmental models. Models accounting for land use explained the largest proportion of the variance in migration rates between sites. A greater number of irrigation channels leading into a site was associated with an increase in the site's propensity to both attract and retain snails.

Conclusions/significance: Our findings have important implications for controlling the geographic spread of schistosomiasis in China, through improved understanding of the dispersal capacity of the parasite's intermediate host.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Migration*
  • Animals
  • Bayes Theorem
  • China / epidemiology
  • Disease Vectors
  • Ecology
  • Environment
  • Genotype
  • Geography
  • Humans
  • Infection Control
  • Phylogeny
  • Schistosoma japonicum / genetics
  • Schistosoma japonicum / isolation & purification
  • Schistosomiasis / epidemiology
  • Schistosomiasis / parasitology
  • Schistosomiasis / prevention & control
  • Schistosomiasis / transmission*
  • Schistosomiasis japonica / epidemiology
  • Schistosomiasis japonica / prevention & control
  • Schistosomiasis japonica / transmission*
  • Snails / genetics*
  • Snails / parasitology
  • Snails / physiology*