Diverging patterns of introgression from Schistosoma bovis across S. haematobium African lineages

Abstract

Hybridization is a fascinating evolutionary phenomenon that raises the question of how species maintain their integrity. Inter-species hybridization occurs between certain Schistosoma species that can cause important public health and veterinary issues. In particular hybrids between Schistosoma haematobium and S. bovis associated with humans and animals respectively are frequently identified in Africa. Recent genomic evidence indicates that some S. haematobium populations show signatures of genomic introgression from S. bovis. Here, we conducted a genomic comparative study and investigated the genomic relationships between S. haematobium, S. bovis and their hybrids using 19 isolates originating from a wide geographical range over Africa, including samples initially classified as S. haematobium (n = 11), S. bovis (n = 6) and S. haematobium x S. bovis hybrids (n = 2). Based on a whole genomic sequencing approach, we developed 56,181 SNPs that allowed a clear differentiation of S. bovis isolates from a genomic cluster including all S. haematobium isolates and a natural S. haematobium-bovis hybrid. All the isolates from the S. haematobium cluster except the isolate from Madagascar harbored signatures of genomic introgression from S. bovis. Isolates from Corsica, Mali and Egypt harbored the S. bovis-like Invadolysin gene, an introgressed tract that has been previously detected in some introgressed S. haematobium populations from Niger. Together our results highlight the fact that introgression from S. bovis is widespread across S. haematobium and that the observed introgression is unidirectional.

Natural Intra- and Interclade Human Hybrid Schistosomes in Africa with Considerations on Prevention through Vaccination

“…Based on parasites recovered from Niger, it has been estimated that introgression occurred around 240.6 years ago (range: −107.8 to −612.5 years) [ 82 ]. The ancestral origin of these hybrids was confirmed with parasites originating from several settings across Western Africa [ 49 ].…”

“…Recombinants are characterized by heterotic alterations, speciations, neo-functionalization and adaptations, called hybrid vigor [ 49 ]. This affects e.g., virulence, transmission, infectivity, pathologies, maturation, fecundity, host spectrum and preference, e.g., extended host range of Shx S. mattheei (Sma) hybrids to sheep, and ShxSb hybrids to non-human primates and rodents, and chemotherapeutic efficacy, e.g., diminished response to oxamniquine if Sma interacts with Sh [ 5 , 13 , 39 , 44 , 50 , 51 , 52 , 53 , 54 , 55 ].…”

“…This affects e.g., virulence, transmission, infectivity, pathologies, maturation, fecundity, host spectrum and preference, e.g., extended host range of Shx S. mattheei (Sma) hybrids to sheep, and ShxSb hybrids to non-human primates and rodents, and chemotherapeutic efficacy, e.g., diminished response to oxamniquine if Sma interacts with Sh [ 5 , 13 , 39 , 44 , 50 , 51 , 52 , 53 , 54 , 55 ]. Taken together, this may result in the expansion to new geographic habitats, and homogenization or progressive, competitive extinction of species as seen for S. guineensis (Sg) in Cameroon, and ultimately the emergence of new diseases [ 49 ].…”

“…Hybrids are detected either when the biparentally inherited ITS marker shows heterozygous pattern at specific mutation points and/or if ITS and COX markers give discordant results in species assignation. Recent developments in single nucleotide polymorphisms (SNPs) markers on both, Sh and Sb, will certainly advance the characterization of genomic properties of hybrids in the near future [ 49 ].…”

“…Three haplotypes detected among ITS2 fragments showed 99.98% sequence identity; haplotype-1 and -2 harbored Sh SNPs, i.e., guanine-cytosine-guanine, at the polymorphic positions 25, 80 and 130, whereas haplotype-3 harbored a single SNP, i.e., adenine, of either Sb, Sc or Sg at position 130. Pairing of male Sh with female Sb and subsequent backcrossing with parental Sh likely explains the majority of COX1 and ITS2 patterns observed [ 49 ]. Of note is the shared Sh-ITS2xSb-COX1 behavior between Sô-Tchanhoué and Corsica strains though it does not explain its recurrence despite established B. contortus , B. truncatus and Planorbarius metidjensis hosts throughout Southern Europe [ 90 , 91 ].…”