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

Abstract

BackgroundAnthropogenic 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 FindingsParasites 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/SignificanceOur 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.

The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals

“…For example, it has been shown that the construction of large dams has led to increases in human schistosomiasis in China, Cote d’Ivoire, Egypt, Ethiopia, Senegal [104], and Sudan, amongst others [105–107]. Dam spillways are known to serve as breeding sites for blackflies [108], and the construction of dams can lead to complex changes in habitat, which in addition to movement of non-immune populations and snails into the area can lead to transmission hotspots [109].…”

A Darwinian outlook on schistosomiasis elimination

“…A study on S. mansoni infecting wild rat (Rattus rattus) showed that the asexual amplification within snails did not play an important role in the total genetic diversity of the adult stages [40]. Models furthermore confirmed that the effect of the clonal amplification phase on adult population genetics is small when there are high levels of parasite gene flow [41,42], which has been reported within most natural schistosome populations [43][44][45][46]. Hence, we believe that ignoring the asexual stage in the snail will not affect the outcome of our study when migration is sufficiently large.…”

Climate Change and the Neglected Tropical Diseases

“…Food demand and production are likely to change considerably in coming decades due to population growth, direct and indirect effects of climate change (Valin et al, 2014). Various large-scale effects have been speculated including risks to global food security (Wheeler and von Braun, 2013) through, e.g., loss of freshwater for irrigation (Elliott et al, 2014).…”