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

Abstract

BackgroundSchistosomes 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 FindingsLarge-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/SignificanceThese 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.

Roadmap to a One Health agenda 2030.

“…It is typically targeted with mass drug administration programmes, provision of safe water and sanitation, molluscicide use and education programmes to highlight risks [113]. However, recent changes in the species evolution and changing transmission ecology, including zoonotic spill overs and multi-host pathogenicity and hybridization have been demonstrated [114][115][116][117]. Thus, in the ever changing world of human and animal population growth, anthropogenic environmental changes, globalized movements of livestock and humans, the previous narrow, anthropocentric or disjointed sectoral approach to the control of schistosomiasis in humans will now require a paradigm shift, taking a wider view through an OH approach.…”

The contribution of mass drug administration to global health: past, present and future

“…S. mansoni pairings with S. haematobium [48] Mixed species pairings and introgressed viable hybrid progeny, e.g. S. haematobium pairings with S. bovis and/or S. currasoni [72], e.g. Ascaris lumbrocoides pairings with A. suum [76] rstb.royalsocietypublishing.org Phil.…”

“…Non-human primates, rodents and insectivores are responsible for human S. mansoni infections in some regions of Africa and the Caribbean [95 -97]. While S. haematobium was believed to be essentially an exclusively human-specific parasite [98], recent molecular studies have confirmed bidirectional hybridization between S. haematobium with the animal (cattle, goat and sheep) schistosome species S. bovis [99] and S. curassoni among infected children in West Africa [72]. The implications of zoonotic hybrids on transmission potential are substantial, particularly in terms of the potential for increased definitive and intermediate host ranges, hybrid vigour, as well as differential PZQ susceptibilities.…”

Changements globaux et infections parasitaires à mollusques vecteurs

“…Au-delà de l'hôte vecteur, c'est-à-dire du mollusque, on peut également se poser la question de la capacité de cet hybride à infecter les ruminants. Les études menées au Sénégal n'ont pas mis en évidence la présence de l'hybride dans les vaisseaux mésentériques de la vache (qui est le siège de S. bovis) [7]. Cependant, les auteurs n'ont pas analysé le système vasculaire de la vessie (siège de S. haematobium) ni les produits excrétés par les animaux (urine et/ ou fèces).…”

“…L'hybridation peut également augmenter la virulence du parasite vis-à-vis de son hôte vertébré. Expérimentalement, dans le modèle utilisant le hamster comme hôte définitif, 30 % des cercaires 4 [4], où ils sont largement répandus dans la population humaine (88 % des patients, localisés sur la quasi-totalité du territoire sénégalais, portent le parasite hybride) [7]. Des cas d'hybridations naturelles entre espèces de schistosome sont en fait de plus en plus souvent recensés chez l'homme : S. mansoni (agent de la bilharziose intestinale humaine) et S. rodhaini (agent de la bilharziose de rongeurs) au Kenya ; S. mansoni et S. haematobium au Séné-gal ; S. guineensis et S. haematobium au Bénin ou au Cameroun.…”