Morphological and genomic characterisation of the Schistosoma hybrid infecting humans in Europe reveals admixture between Schistosoma haematobium and Schistosoma bovis

Abstract

Schistosomes cause schistosomiasis, the world's second most important parasitic disease after malaria in terms of public health and social-economic impacts. A peculiar feature of these dioecious parasites is their ability to produce viable and fertile hybrid offspring. Originally only present in the tropics, schistosomiasis is now also endemic in southern Europe. Based on the analysis of two genetic markers the European schistosomes had previously been identified as hybrids between the livestock- and the human-infective species Schistosoma bovis and Schistosoma haematobium, respectively. Here, using PacBio long-read sequencing technology we performed genome assembly improvement and annotation of S. bovis, one of the parental species for which no satisfactory genome assembly was available. We then describe the whole genome introgression levels of the hybrid schistosomes, their morphometric parameters (eggs and adult worms) and their compatibility with two European snail strains used as vectors (Bulinus truncatus and Planorbarius metidjensis). Schistosome-snail compatibility is a key parameter for the parasites life cycle progression, and thus the capability of the parasite to establish in a given area. Our results show that this Schistosoma hybrid is strongly introgressed genetically, composed of 77% S. haematobium and 23% S. bovis origin. This genomic admixture suggests an ancient hybridization event and subsequent backcrosses with the human-specific species, S. haematobium, before its introduction in Corsica. We also show that egg morphology (commonly used as a species diagnostic) does not allow for accurate hybrid identification while genetic tests do.

Fig 1. Egg morphologies of the pure parental species and the European S. haematobium-bovis hybrids.

Eggs 1 and 2 show typical morphologies of S. haematobium (elliptical with a terminal spine) and S. bovis (spindle shape with a terminal spine), respectively from laboratory isolates. Eggs 3–9 show the egg morphology of the European S. haematobium-bovis hybrid schistosome. While most eggs were of a typical S. haematobium morphotype (3–7), there was a high variability in the morphologies and near 10% (4/44) of eggs were non-typical (8–9).

Fig 2. Morphological observations of the European male hybrid adult worms.

(A) Whole parasite body showing the oral sucker, acetabulum (ventral sucker) and gynaecophoral canal; (B) Frontal view of the anterior region showing the oral sucker and acetabulum (ventral sucker) in detail; (C) Dorso-lateral view of the spines and tubercles on the parasite surface.

Fig 3. Morphological observations of the European female hybrid adult worms.

(A) Lateral view of whole parasite body showing oral sucker, acetabulum (ventral sucker), ovary and vitellaria; (B) Frontal view of anterior region showing oral sucker, acetabulum (ventral sucker) in detail; (C) Dorso-lateral view of two eggs inside female uterus.