Extant interspecific hybridization among trematodes within the Schistosoma haematobium species complex in Nigeria

Abstract

BackgroundNatural interspecific hybridization between the human parasite (Schistosoma haematobium [Sh]) and bovine parasites (S. bovis [Sb], S. curassoni [Sc]) is increasingly reported in Africa. We developed a multi-locus PCR DNA-Seq strategy that amplifies two unlinked nuclear (transITS, BF) and two linked organellar genome markers (CO1, NAD5) to genotype S. haematobium eggs collected from infected people in Ile Oluji/Oke Igbo, Ondo State (an agrarian community) and Kachi, Jigawa State (a pastoral community) in Southwestern and Northern Nigeria, respectively. Principal FindingsWe applied this methodology against 57 isolates collected from a total of 219 participants. All patients from Jigawa state were infected with just one of two haplotypes of an S. haematobium x S. bovis hybrid based on sequences obtained at CO1, NAD5, transITS and BF markers. Whereas samples collected from Ondo state were varied. Mitonuclear discordance was observed in all 17 patients, worms possessed an Sb mitochondrial genome but one of four different haplotypes at the nuclear markers, either admixed (heterozygous between Sh x Sc or Sh x Sb) at both markers (n=10), Sh at BF and admixed at transITS (Sh x Sc) (n=5), admixed (Sh x Sc) at BF and homozygous Sc at transITS (n=1) or homozygous Sh at BF and homozygous Sc at transITS (n=1). SignificancePrevious work suggested that zoonotic transmission of S. bovis in pastoral communities, where humans and animals share a common water source, is a driving factor facilitating interspecific hybridization. However, our data showed that all isolates were hybrids, with greater diversity identified in Southwestern Nigeria, a non-pastoral site. Further, one patient possessed an S. bovis mitochondrial genome but was homozygous for S. haematobium at BF and homozygous for S. curassoni at transITS supporting at least two separate backcrosses in its origin, suggesting that interspecific hybridization may be an ongoing process. Author SummaryInterspecific hybridization between trematode parasites poses serious health risks to humans. Many systems have shown possible hybridization between different schistosome species. As evidence of natural hybridization between human S. haematobium and animal S. bovis or S. curassoni has grown in recent years, epidemiological surveys across potential hybrid zones are required, particularly in endemic African regions. According to several reports, indiscriminate human-animal water contact is a major factor contributing to hybridization of human and animal schistosomes. We collected and genotyped 57 parasite isolates from pastoral and non-pastoral communities in Kachi, Jigawa state, and Ile Oluji/Oke Igbo, Ondo state, Nigeria to screen for hybrids. In both sites, we found Schistosoma hybrids with mitonuclear discordance and repeated backcrossing between S. haematobium, S. bovis, and S. curassoni. Contrary to previous reports, Schistosoma hybrids appear to be widespread and not solely dependent on human-animal water interactions.