Reconstructing Colonization Dynamics of the Human Parasite Schistosoma mansoni following Anthropogenic Environmental Changes in Northwest Senegal

PLoS Negl Trop Dis. 2015 Aug 14;9(8):e0003998. doi: 10.1371/journal.pntd.0003998. eCollection 2015 Aug.

Abstract

Background: Anthropogenic environmental changes may lead to ecosystem destabilization and the unintentional colonization of new habitats by parasite populations. A remarkable example is the outbreak of intestinal schistosomiasis in Northwest Senegal following the construction of two dams in the '80s. While many studies have investigated the epidemiological, immunological and geographical patterns of Schistosoma mansoni infections in this region, little is known about its colonization history.

Methodology/principal findings: Parasites were collected at several time points after the disease outbreak and genotyped using a 420 bp fragment of the mitochondrial cytochrome c oxidase subunit 1 gene (cox1) and nine nuclear DNA microsatellite markers. Phylogeographic and population genetic analyses revealed the presence of (i) many genetically different haplotypes at the non-recombining mitochondrial marker and (ii) one homogenous S. mansoni genetic group at the recombining microsatellite markers. These results suggest that the S. mansoni population in Northwest Senegal was triggered by intraspecific hybridization (i.e. admixture) between parasites that were introduced from different regions. This would comply with the extensive immigration of infected seasonal agricultural workers from neighboring regions in Senegal, Mauritania and Mali. The spatial and temporal stability of the established S. mansoni population suggests a swift local adaptation of the parasite to the local intermediate snail host Biomphalaria pfeifferi at the onset of the epidemic.

Conclusions/significance: Our results show that S. mansoni parasites are very successful in colonizing new areas without significant loss of genetic diversity. Maintaining high levels of diversity guarantees the adaptive potential of these parasites to cope with selective pressures such as drug treatment, which might complicate efforts to control the disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bayes Theorem
  • Cluster Analysis
  • DNA, Helminth
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism
  • Environment*
  • Gene Expression Regulation, Enzymologic
  • Genetic Variation
  • Human Activities*
  • Humans
  • Microsatellite Repeats
  • Phylogeography
  • Population Dynamics*
  • Schistosoma mansoni / enzymology
  • Schistosoma mansoni / genetics
  • Schistosoma mansoni / physiology*
  • Schistosomiasis mansoni / epidemiology
  • Schistosomiasis mansoni / parasitology*
  • Senegal / epidemiology

Substances

  • DNA, Helminth
  • Electron Transport Complex IV

Grants and funding

FVdB benefited from a doctoral fellowship (grant number VLADOC2010-07) from the Flemish Interuniversity Council (VLIR-UOS; www.vliruos.be). TH and MHDL benefited from a postdoctoral fellowship (grant numbers 1.2.668.11.N.01 and 12E2315N resp.) from the Research Foundation-Flanders (FWO Vlaanderen; www.fwo.be). Research benefited from a Research Grant (grant number G.0552.10) of the Research Foundation - Flanders to TH, FAMV and KP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.