Introgressive Hybridization of Schistosoma haematobium Group Species in Senegal: Species Barrier Break Down between Ruminant and Human Schistosomes

Abstract

Background

Schistosomes are dioecious parasitic flatworms, which live in the vasculature of their mammalian definitive hosts. They are the causative agent of schistosomiasis, a disease of considerable medical and veterinary importance in tropical and subtropical regions. Schistosomes undergo a sexual reproductive stage within their mammalian host enabling interactions between different species, which may result in hybridization if the species involved are phylogenetically close. In Senegal, three closely related species in the Schistosoma haematobium group are endemic: S. haematobium, which causes urogenital schistosomiasis in humans, and S. bovis and S. curassoni, which cause intestinal schistosomiasis in cows, sheep and goats.

Methodology/Principal Findings

Large-scale multi-loci molecular analysis of parasite samples collected from children and domestic livestock across Senegal revealed that interactions and hybridization were taking place between all three species. Evidence of hybridization between S. haematobium/ S. curassoni and S. haematobium/ S. bovis was commonly found in children from across Senegal, with 88% of the children surveyed in areas of suspected species overlap excreting hybrid miracidia. No S. haematobium worms or hybrids thereof were found in ruminants, although S. bovis and S. curassoni hybrid worms were found in cows. Complementary experimental mixed species infections in laboratory rodents confirmed that males and females of each species readily pair and produce viable hybrid offspring.

Conclusions/Significance

These data provide indisputable evidence for: the high occurrence of bidirectional hybridization between these Schistosoma species; the first conclusive evidence for the natural hybridisation between S. haematobium and S. curassoni; and demonstrate that the transmission of the different species and their hybrids appears focal. Hybridization between schistosomes has been known to influence the disease epidemiology and enhance phenotypic characteristics affecting transmission, morbidity and drug sensitivity. Therefore, understanding and monitoring such inter-species interactions will be essential for optimizing and evaluating control strategies across such potential hybrid zones.

Author Summary

Schistosome blood flukes are transmitted through water contact and cause a severe debilitating disease in humans and their livestock. Understanding the biology and epidemiology of these parasites is essential to enable the development of better control strategies in endemic areas. Several species of schistosome exist and species barriers are normally maintained by differences in ecology, host specificity, and evolutionary history. However, hybridization between closely related species can occur if parasites infect the same definitive host. Here we report on the introgression between a human ( S. haematobium) and two ruminant schistosomes ( S. bovis and S. curassoni), the prevalence and distribution of their hybrids and the novel evidence for the presence of S. haematobium/ S. curassoni hybrids in Senegalese children. Modern sampling and genotyping techniques have brought to light the extent of these hybridization events which could have been facilitated by the natural progression in farming, population (both human and livestock) movements and expansion, as well as changes in snail distribution, creating areas of sympatric transmission. Hybridization can lead to phenotypic characteristics that can influence disease epidemiology and control success, highlighting the importance of monitoring these evolving hybrid zones.