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

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.     

Bidirectional Introgressive Hybridization between a Cattle and Human Schistosome Species

Schistosomiasis is a disease of great medical and veterinary importance in tropical and subtropical regions, caused by parasitic flatworms of the genus Schistosoma (subclass Digenea). Following major water development schemes in the 1980s, schistosomiasis has become an important parasitic disease of children living in the Senegal River Basin (SRB). During molecular parasitological surveys, nuclear and mitochondrial markers revealed unexpected natural interactions between a bovine and human Schistosoma species: S. bovis and S. haematobium, respectively. Hybrid schistosomes recovered from the urine and faeces of children and the intermediate snail hosts of both parental species, Bulinus truncatus and B. globosus, presented a nuclear ITS rRNA sequence identical to S. haematobium, while the partial mitochondrial cox1 sequence was identified as S. bovis. Molecular data suggest that the hybrids are not 1st generation and are a result of parental and/or hybrid backcrosses, indicating a stable hybrid zone. Larval stages with the reverse genetic profile were also found and are suggested to be F1 progeny. The data provide indisputable evidence for the occurrence of bidirectional introgressive hybridization between a bovine and a human Schistosoma species. Hybrid species have been found infecting B. truncatus, a snail species that is now very abundant throughout the SRB. The recent increase in urinary schistosomiasis in the villages along the SRB could therefore be a direct effect of the increased transmission through B. truncatus. Hybridization between schistosomes under laboratory conditions has been shown to result in heterosis (higher fecundity, faster maturation time, wider intermediate host spectrum), having important implications on disease prevalence, pathology and treatment. If this new hybrid exhibits the same hybrid vigour, it could develop into an emerging pathogen, necessitating further control strategies in zones where both parental species overlap.     

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

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.     

Conservation of protein kinase a catalytic subunit sequences in the schistosome pathogens of humans

cAMP-dependent protein kinases (PKAs) are central mediators of cAMP signaling in eukaryotic cells. Previously we identified a cDNA which encodes for a PKA catalytic subunit (PKA-C) in Schistosoma mansoni (SmPKA-C) that is required for adult schistosome viability in vitro. As such, SmPKA-C could potentially represent a novel schistosome chemotherapeutic target. Here we sought to identify PKA-C subunit orthologues in the other medically important schistosome species, Schistosoma haematobium and Schistosoma japonicum, to determine the degree to which this potential target is conserved and could therefore be exploited for the treatment of all forms of schistosomiasis. We report the identification of PKA-C subunit orthologues in S. haematobium and S. japonicum (ShPKA-C and SjPKA-C, respectively) and show that PKA-C orthologues are highly conserved in the Schistosoma, with over 99% amino acid sequence identity shared among the three human pathogens we examined. Furthermore, we show that the recently published Schistosoma mansoni and S. japonicum genomes contain sequences encoding for several putative PKA substrates with homology to those found in Homo sapiens, Caenorhabditis elegans, and Saccharomyces cerevisiae.     

Mitochondrial gene order change in Schistosoma (Platyhelminthes: Digenea: Schistosomatidae)

In the flatworm genus Schistosoma, species of which include parasites of biomedical and veterinary importance, mitochondrial gene order is radically different in some species. A PCR-based survey of 19 schistosomatid spp. established which of 14 Schistosoma spp. have the ancestral (plesiomorphic) or derived gene order condition. A phylogeny for Schistosoma was estimated and used to infer the origin of the gene order change which is present in all members of a clade containing Schistosoma incognitum and members of the traditionally recognised Schistosoma indicum, Schistosoma mansoni and Schistosoma haematobium spp. groups. Schistosoma turkestanicum, with the plesiomorphic gene order state, is sister to this clade. Common interval analysis suggests change in gene order, from ancestral to derived, consisted of two sequential transposition events: (a) nad1_nad3 to nad3_nad1 and (b) [atp6,nad2]_[nad3,nad1,cox1,rrnL,rrnS,cox2,nad6] to [nad3,nad1,cox1,rrnL,rrnS,cox2,nad6]_[atp6,nad2], where gene order of fragments within square brackets remain unchanged. Gene order change is rare in parasitic flatworms and is a robust synapomorphy for schistosome spp. that exhibit it. The schistosomatid phylogeny casts some doubt on the origin of Schistosoma (Asian or African), highlights the propensity for species to host switch amongst mammalian (definitive) hosts, and indicates the likely importance of snail (intermediate) hosts in determining and defining patterns of schistosome radiation and continental invasion. Mitogenomic sampling of Schistosoma dattai and Schistosoma harinasutai to determine gene order, and within key species, especially S. turkestanicum and S. incognitum, to determine ancestral ranges, may help discover the geographic origins of gene order change in the genus. Samples of S. incognitum from India and Thailand suggest this taxon may include cryptic species.     

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

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.     

Transmission and diversity of Schistosoma haematobium and S. bovis and their freshwater intermediate snail hosts Bulinus globosus and B. nasutus in the Zanzibar Archipelago,United Republic of Tanzania

BackgroundThe Zanzibar Archipelago (Pemba and Unguja islands) is targeted for the elimination of human urogenital schistosomiasis caused by infection with Schistosoma haematobium where the intermediate snail host is Bulinus globosus. Following multiple studies, it has remained unclear if B. nasutus (a snail species that occupies geographically distinct regions on the Archipelago) is involved in S. haematobium transmission on Zanzibar. Additionally, S. haematobium was thought to be the only Schistosoma species present on the Zanzibar Archipelago until the sympatric transmission of S. bovis, a parasite of ruminants, was recently identified. Here we re-assess the epidemiology of schistosomiasis on Pemba and Unguja together with the role and genetic diversity of the Bulinus spp. involved in transmission.Methodology/Principal findingsMalacological and parasitological surveys were conducted between 2016 and 2019. In total, 11,116 Bulinus spp. snails were collected from 65 of 112 freshwater bodies surveyed. Bulinus species identification were determined using mitochondrial cox1 sequences for a representative subset of collected Bulinus (n = 504) and together with archived museum specimens (n = 6), 433 B. globosus and 77 B. nasutus were identified. Phylogenetic analysis of cox1 haplotypes revealed three distinct populations of B. globosus, two with an overlapping distribution on Pemba and one on Unguja. For B. nasutus, only a single clade with matching haplotypes was observed across the islands and included reference sequences from Kenya. Schistosoma haematobium cercariae (n = 158) were identified from 12 infected B. globosus and one B. nasutus collected between 2016 and 2019 in Pemba, and cercariae originating from 69 Bulinus spp. archived in museum collections. Schistosoma bovis cercariae (n = 21) were identified from seven additional B. globosus collected between 2016 and 2019 in Pemba. By analysing a partial mitochondrial cox1 region and the nuclear ITS (1–5.8S-2) rDNA region of Schistosoma cercariae, we identified 18 S. haematobium and three S. bovis haplotypes representing populations associated with mainland Africa and the Indian Ocean Islands (Zanzibar, Madagascar, Mauritius and Mafia).Conclusions/SignificanceThe individual B. nasutus on Pemba infected with S. haematobium demonstrates that B. nasutus could also play a role in the local transmission of S. haematobium. We provide preliminary evidence that intraspecific variability of S. haematobium on Pemba may increase the transmission potential of S. haematobium locally due to the expanded intermediate host range, and that the presence of S. bovis complicates the environmental surveillance of schistosome infections.     

Genomic evidence of contemporary hybridization between Schistosoma species

Hybridization between different species of parasites is increasingly being recognised as a major public and veterinary health concern at the interface of infectious diseases biology, evolution, epidemiology and ultimately control. Recent research has revealed that viable hybrids and introgressed lineages between Schistosoma spp. are prevalent across Africa and beyond, including those with zoonotic potential. However, it remains unclear whether these hybrid lineages represent recent hybridization events, suggesting hybridization is ongoing, and/or whether they represent introgressed lineages derived from ancient hybridization events. In human schistosomiasis, investigation is hampered by the inaccessibility of adult-stage worms due to their intravascular location, an issue which can be circumvented by post-mortem of livestock at abattoirs for Schistosoma spp. of known zoonotic potential. To characterise the composition of naturally-occurring schistosome hybrids, we performed whole-genome sequencing of 21 natural livestock infective schistosome isolates. To facilitate this, we also assembled a de novo chromosomal-scale draft assembly of Schistosoma curassoni. Genomic analyses identified isolates of S. bovis, S. curassoni and hybrids between the two species, all of which were early generation hybrids with multiple generations found within the same host. These results show that hybridization is an ongoing process within natural populations with the potential to further challenge elimination efforts against schistosomiasis.     

Schistosoma mansoni: antigenic characterization of malate dehydrogenase isoenzymes and use in the defined antigen substrate spheres (DASS) system.

Immunoelectrophoresis of Schistosoma mansoni homogenates against mouse antisera resulted in only one precipitation line, which showed malate dehydrogenase activity. Immunoprecipitins against schistosomal malate dehydrogenase were also demonstrated in sera from individuals with schistosomiasis. Analysis by the double-diffusion method showed that malate dehydrogenase antigens in S. mansoni, S. haematobium, and S. bovis are immunologically indistinguishable. Immunoelectrophoresis of isolated mitochondrial and cytoplasmic malate dehydrogenase, showed that only the mitochondrial enzyme is able to form a malate dehydrogenase active precipitation line. Rabbit antisera directed against purified mitochondrial malate dehydrogenase showed a reaction with the enzyme as judge by immunoelectrophoresis. A purified mitochondrial malate dehydrogenase preparation, coupled to Sepharose 4B, was used in the defined antigen substrate spheres (DASS) test. Sera from experimentally infected mice contained considerably higher levels of antibodies against the mitochondrial malate dehydrogenase preparation than sera from infected individuals.     

Carbohydrate metabolism in adult schistosomes of different strains and species

In this comparative study the carbohydrate metabolism of Schistosoma japonicum, S. haematobium, S. intercalatum, S. bovis and three strains of S. mansoni was investigated. No large differences were found in the protein and glycogen contents of all species involved. In all species investigated, lactate was the main end product of carbohydrate breakdown. However, all parasites degraded part of the glucose to CO2 via the Krebs cycle. No difference was observed in the contribution of this aerobic process to energy production in the three strains of S. mansoni investigated. The differences in Krebs-cycle activity between the five schistosome species investigated were very small. Therefore, this study refutes the idea that significant differences exist in the carbohydrate metabolism of various schistosome species or strains.     

Introgressive hybridization of human and rodent schistosome parasites in western Kenya

Hybridization and introgression can have important consequences for the evolution, ecology and epidemiology of pathogenic organisms. We examined the dynamics of hybridization between a trematode parasite of humans, Schistosoma mansoni, and its sister species, S. rodhaini, a rodent parasite, in a natural hybrid zone in western Kenya. Using microsatellite markers, rDNA and mtDNA, we showed that hybrids between the two species occur in nature, are fertile and produce viable offspring through backcrosses with S. mansoni. Averaged across collection sites, individuals of hybrid ancestry comprised 7.2% of all schistosomes collected, which is a large proportion given that one of the parental species, S. rodhaini, comprised only 9.1% of the specimens. No F1 individuals were collected and all hybrids represented backcrosses with S. mansoni that were of the first or successive generations. The direction of introgression appears highly asymmetric, causing unidirectional gene flow from the rodent parasite, S. rodhaini, to the human parasite, S. mansoni. Hybrid occurrence was seasonal and most hybrids were collected during the month of September over a 2-year period, a time when S. rodhaini was also abundant. We also examined the sex ratios and phenotypic differences between the hybrids and parental species, including the number of infective stages produced in the snail host and the time of day the infective stages emerge. No statistical differences were found in any of these characteristics, and most of the hybrids showed an emergence pattern similar to that of S. mansoni. One individual, however, showed a bimodal emergence pattern that was characteristic of both parental species. In conclusion, these species maintain their identity despite hybridization, although introgression may cause important alterations of the biology and epidemiology of schistosomiasis in this region.     

Schistosomiasis mansoni, haematobia, and japonica in hamsters: liver granuloma measurements

Differences in the granulomatous response of hamsters infected with Schistosoma mansoni, Schistosoma haematobium, or Schistosoma japonicum were studied by measuring granulomas formed around eggs in the livers at 1, 3, 5, 11, and 19 week intervals after patency of the infections. For each species, the mean diameters of both granulomas containing only 1 egg and granulomas selected at random were determined. The mean volume of single egg granulomas in S. mansoni-infected hamsters was greater than in those with other species at all time intervals studied. The decrease in single egg granuloma size with time occurred more gradually in S. mansoni infections. The mean volume of granulomas measured at random was greatest in S. japoracum-infected animals at 1, 3, and 11 weeks after patency; was greatest in S. haematobium-iufected. hamsters at 5 and 19 weeks; and was least in S. mansoni-infected hamsters at all time periods. During the 19 week period following patency, the mean volume of randomly measured granulomas increased with time in S. haematobium infections, decreased gradually in S. mansoni infections, and decreased markedly in S. japonicum infections. Multi-egg granulomas represented 2–6% of all granulomas measured in S. mansoni infections, 38–68% in S. haematobium infections, and 20–53% in S. japonicum infections. An estimated proportion of the liver occupied by granulomas, i.e., a lesion-to-tissue ratio, was computed. There was no consistent difference in this ratio among the 3 species when the data were grouped in comparable intervals of mean number of eggs per g of liver. The lesion-to-tissue ratio increased with increasing numbers of eggs per g of liver. The host response of hamsters to these 3 species of schistosomes differed markedly even at comparable levels of eggs per g of liver. This study provides further evidence of an intrinsic qualitative difference in the eggs of the 3 species. The species of eggs present in tissues apparently has greater influence on the host response than does the quantity of eggs present.     

Pattern of cercarial emergence of Schistosoma curassoni from Niger and comparison with three sympatric species of schistosomes.

The emergence pattern of Schistosoma curassoni cercariae from Bulinus umbilicatus, whose adult worms parasitize bovine, caprine, and ovine ungulates in Niger, is of a circadian type with a mean emission time at 0855 hr +/- 1 hr 6 min, characteristic of the schistosome species parasitizing domestic or wild cattle. The comparison of this cercarial emergence pattern with those of the other 3 sympatric species of schistosomes (Schistosoma haematobium, Schistosoma bovis, and Schistosoma mansoni) shows a significant difference between the chronobiology of the cercariae infective for human and those infective for bovine hosts. This difference may improve epidemiological surveys based on snail prevalences by allowing the distinction between bulinids infected with human and bovine parasites.     

A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis

In light of the recently described human schistosome Schistosoma guineensis and recent phylogenetic studies of the genus Schistosoma, a revision of the interrelationships of the members of this genus is needed. This paper adds to previous phylogenetic studies on the family Schistosomatidae and offers the most up to date and robust phylogeny of the group based on complete small and large nuclear subunit rRNA genes and partial mitochondrial cox1, incorporating most of the 21 species of Schistosoma. Our findings show that the group retains the same topology as that resolved in previous studies except Schistosoma margrebowiei was resolved as the sister taxon to all others in the Schistosoma haematobium species group and S. guineensis was placed as sister species to both Schistosoma bovis and Schistosoma curassoni. The S. haematobium species group contains eight species of which many are of significant medical and veterinary importance. Additionally, many of these species have been shown to hybridise both in the wild and experimentally, making the correct identification and recognition of species very important. A pairwise comparison of cox1 among Schistosoma species suggests this gene alone would fail as a reliable barcode for species identification. Phylogenetic results clearly treat Schistosoma intercalatum and S. guineensis as separate taxa with each more closely related evolutionarily to S. haematobium than to each other. The study also highlights the problems associated with wrongly attributed sequences on public databases such as GenBank.     

Genetic Diversity of Schistosoma haematobium Eggs Isolated from Human Urine in Sudan

The genetic diversity of Schistosoma haematobium remains largely unstudied in comparison to that of Schistosoma mansoni. To characterize the extent of genetic diversity in S. haematobium among its definitive host (humans), we collected S. haematobium eggs from the urine of 73 infected schoolchildren at 5 primary schools in White Nile State, Sudan, and then performed a randomly amplified polymorphic DNA marker ITS2 by PCR-RFLP analysis. Among 73 S. haematobium egg-positive cases, 13 were selected based on the presence of the S. haematobium satellite markers A4 and B2 in their genomic DNA, and used for RFLP analysis. The 13 samples were subjected to an RFLP analysis of the S. haematobium ITS2 region; however, there was no variation in size among the fragments. Compared to the ITS2 sequences obtained for S. haematobium from Kenya, the nucleotide sequences of the ITS2 regions of S. haematobium from 4 areas in Sudan were consistent with those from Kenya (> 99%). In this study, we demonstrate for the first time that most of the S. haematobium population in Sudan consists of a pan-African S. haematobium genotype; however, we also report the discovery of Kenyan strain inflow into White Nile, Sudan.     

Mitochondrial DNA sequence and gene order of the Sri Lankan Schistosoma nasale is affiliated to the African/Indian group

A 1.9 kb nucleotide sequence of part of the mitochondrial (mt) genome covering the cox1-trnT-rrnL-trnC-rrnS region, and the order of the remaining mitochondrial protein-coding genes for S. nasale of Sri Lankan origin, has been determined for analysis of the possible placement of this species in the genus Schistosoma. The gene order of this species is similar to that of the African and Indian Schistosoma species, but strikingly different from the East Asian species. Analysis of an alignment of the 1.9 kb sequence with available sequences from other schistosomes indicated affinities with S. spindale (found in Sri Lanka) and African species (in particular S. intercalatum and S. haematobium). Phylogenetic trees inferred from the alignment including 1 kb of RNA (transfer RNA and ribosomal RNA) sequence for 8 other Schistosoma spp. and Fasciola hepatica as an out-group revealed that S. nasale is placed proximally to S. spindale, S. intercalatum, S. haematobium and S. mansoni in the African sub-group while the East Asian species are more distant. S. incognitum lies basal to the combined African/Indian clade. The mtDNA analysis strongly supports the hypothesis that S. nasale is closely affiliated with the African/Indian schistosome group rather than the East Asian Schistosoma species.     

Cytokine Responses to Schistosoma mansoni and Schistosoma haematobium in Relation to Infection in a Co-endemic Focus in Northern Senegal

Background

In Africa, many areas are co-endemic for the two major Schistosoma species, S. mansoni and S. haematobium. Epidemiological studies have suggested that host immunological factors may play an important role in co-endemic areas. As yet, little is known about differences in host immune responses and possible immunological interactions between S. mansoni and S. haematobium in humans. The aim of this study was to analyze host cytokine responses to antigens from either species in a population from a co-endemic focus, and relate these to S. mansoni and S. haematobium infection.

Methodology

Whole blood cytokine responses were investigated in a population in the north of Senegal (n = 200). Blood was stimulated for 72 h with schistosomal egg and adult worm antigens of either Schistosoma species. IL-10, IL-5, IFN-γ, TNF-α, and IL-2 production was determined in culture supernatants. A multivariate (i.e. multi-response) approach was used to allow a joint analysis of all cytokines in relation to Schistosoma infection.

Principal Findings

Schistosoma haematobium egg and worm antigens induced higher cytokine production, suggesting that S. haematobium may be more immunogenic than S. mansoni. However, both infections were strongly associated with similar, modified Th2 cytokine profiles.

Conclusions/Significance

This study is the first to compare S. mansoni and S. haematobium cytokine responses in one population residing in a co-endemic area. These findings are in line with previous epidemiological studies that also suggested S. haematobium egg and worm stages to be more immunogenic than those of S. mansoni.     

Detection of Mycobacterium bovis and Mycobacterium tuberculosis from Cattle: Possible Public Health Relevance

Mycobacterium bovis and Mycobacterium tuberculosis infect both animals and humans. The disease epidemiology by these agents differs in developed and developing countries due to the differences in the implementation of the prevention and control strategies. The present study describes the detection of M. bovis and M. tuberculosis from specimens of lungs and pulmonary lymph nodes of four cattle died in an organized herd of 183 cattle in the state of Himachal Pradesh, India, with inconclusive skin test results. Identification and distinction of these closely related mycobacterial species was done by PCR-RFLP targeting hsp65 gene followed by spacer oligonucleotide typing. Mixed infection of M. bovis and M. tuberculosis was detected in one cattle.     

Low genetic diversity in a snail intermediate host (Biomphalaria pfeifferi Krass, 1848) and schistosomiasis transmission in the Senegal River Basin

Population genetic perturbations of intermediate hosts, often a consequence of human pressure on environmental resources, can precipitate unexpectedly severe disease outbreaks. Such disturbances are set to become increasingly common following range changes concomitant with climate shifts, dwindling natural resources and major infrastructure changes such as hydroprojects. Construction of the Diama dam in the Senegal River Basin (SRB) reduced river salinity, enabling the freshwater snail intermediate host Biomphalaria pfeifferi to rapidly expand its distribution. A serious public health problem ensued, with an epidemic of intestinal schistosomiasis occurring in the previously schistosome‐free Richard‐Toll region within 2 years. The current study aimed to assess the population variability of B. pfeifferi in the SRB, and speculate upon its subsequent impact on host‐parasite interactions following such engineered ecological change. Genetic variation at nine polymorphic microsatellite loci revealed little population differentiation in SRB snails compared with those from natural habitats in Zimbabwe, where Schistosoma mansoni transmission is much lower. ‘Open’ SRB habitats are associated with greater water contact, smaller population sizes and less genetic diversity, with sites downstream of Richard‐Toll showing greater inter‐ and intrapopulation variation, concomitant with less frequent human contact. These observations may be explained by rapid expansion into pristine habitat selecting for high fecundity genotypes at the expense of schistosome resistance, presenting S. mansoni with genetically homogenous highly fecund susceptible populations around the focal point, promoting development of a highly compatible host‐parasite relationship. Longitudinal study of such systems may prove important in predicting public health risks engendered by future environmental engineering projects.