Observations on natural and experimental interactions between Schistosoma bovis and S. curassoni from West Africa.
TL;DR: Viable hybrid parasites were produced in the laboratory and were maintained up until the F4 generation, Comparisons of egg morphology, surface structure of adult male worms and enzyme profiles have been made between experimental hybrid lines and field isolates.
Abstract: Surveys of 332 naturally infected bovines at eight abattoirs in Senegal, The Gambia and Mali were carried out to determine the prevalence of infection with Schistosoma bovis and S. curassoni and to pinpoint areas where the distribution of the species overlap. S. bovis was the commonest schistosome of cattle in Senegal and Mali being found in animals at seven abattoirs, the highest prevalance of 85.1% occurred at Mopti in Mali. S. bovis was the only bovine schistosome observed in The Gambia. S. curassoni was isolated from a cow at Bamako and shown to have similar glucose-6-phosphate dehydrogenase, phosphoglucomutase and acid phosphatase profiles to those described for a Senegalese isolate. Evidence of interaction of S. bovis with S. curassoni was found in cattle from Senegal, at Tambacounda and Kolda, and from Mali, at Bamako and Mopti. A mixed experimental infection of both species in a sheep showed the lack of any specific mate recognition system: identification of the worms was facilitated by analysis of acid phosphatase by isoelectric focusing in polyacrylamide gels. Viable hybrid parasites were produced in the laboratory and were maintained up until the F4 generation. Comparisons of egg morphology, surface structure of adult male worms and enzyme profiles have been made between experimental hybrid lines and field isolates. Possible mechanisms maintaining species integrity are discussed.
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TL;DR: In this article, nuclear and mitochondrial markers revealed unexpected natural interactions between a bovine and human Schistosoma species: S. bovis and S. haematobium.
Abstract: 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.
180 citations
TL;DR: 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.
Abstract: 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.
159 citations
TL;DR: 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.
Abstract: 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.
123 citations
Cites background from "Observations on natural and experim..."
...Rollinson et al. (1990) provided evidence for the hybridisation of S. bovis and S. curassoni in parts of West Africa....
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...References for known hybridisations include A, Southgate and Rollinson (1987), and Southgate et al. (1998) ;B ,Bre´mond et al. (1993) ;C ,Tchuem Tchuente´ et al. (1997), and Rollinson et al., (1990) ; D, Rollinson et al. (1990) ;E ,An˜e´ et al. (1997), and Webster and Southgate (2003) ;F ,Vercruysse et al. (1994)....
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...References for known hybridisations include A, Southgate and Rollinson (1987), and Southgate et al. (1998) ;B ,Bre´mond et al. (1993) ;C ,Tchuem Tchuente´ et al. (1997), and Rollinson et al., (1990); D, Rollinson et al. (1990) ;E ,An˜e´ et al. (1997), and Webster and Southgate (2003) ;F ,Vercruysse et al. (1994)....
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TL;DR: Hybridization of parasites is an emerging public health concern at the interface of infectious disease biology and evolution and can allow for heterospecific (between-species or between-lineage) mate pairings, resulting in parthenogenesis and whole-genome admixture.
Abstract: Hybridization of parasites is an emerging public health concern at the interface of infectious disease biology and evolution. Increasing economic development, human migration, global trade, and climate change are all shifting the geographic distribution of existing human, livestock, companion animal, and wildlife parasites [1–9]. As a result, human populations encounter new infections more frequently, and coinfection by multiple parasites from different lineages or species within individual hosts occurs. Coinfection may have a large impact on the hosts and parasites involved, often as a result of synergistic or antagonistic interactions between parasites [10]. Indeed, mixed-species coinfections have been found to influence parasite establishment, growth, maturation, reproductive success, and/or drug efficacy [11–13]. However, coinfections can allow for heterospecific (between-species or between-lineage) mate pairings, resulting in parthenogenesis (asexual reproduction in which eggs occur without fertilization), introgression (the introduction of single genes or chromosomal regions from one species into that of another through repeated backcrossing), and whole-genome admixture through hybridization [14].
116 citations
TL;DR: The aim here is to highlight the importance of both elucidating disease ecology, including identifying key hosts and tailoring control effort accordingly, and understanding parasite evolution, such as precisely how infectious agents may respond and adapt to anthropogenic change.
Abstract: Understanding the complex population biology and transmission ecology of multihost parasites has been declared as one of the major challenges of biomedical sciences for the 21st century and the Neglected Zoonotic Diseases (NZDs) are perhaps the most neglected of all the Neglected Tropical Diseases (NTDs). Here we consider how multihost parasite transmission and evolutionary dynamics may affect the success of human and animal disease control programmes, particularly neglected diseases of the developing world. We review the different types of zoonotic interactions that occur, both ecological and evolutionary, their potential relevance for current human control activities, and make suggestions for the development of an empirical evidence base and theoretical framework to better understand and predict the outcome of such interactions. In particular, we consider whether preventive chemotherapy, the current mainstay of NTD control, can be successful without a One Health approach. Transmission within and between animal reservoirs and humans can have important ecological and evolutionary consequences, driving the evolution and establishment of drug resistance, as well as providing selective pressures for spill-over, host switching, hybridizations and introgressions between animal and human parasites. Our aim here is to highlight the importance of both elucidating disease ecology, including identifying key hosts and tailoring control effort accordingly, and understanding parasite evolution, such as precisely how infectious agents may respond and adapt to anthropogenic change. Both elements are essential if we are to alleviate disease risks from NZDs in humans, domestic animals and wildlife.
113 citations
Cites background from "Observations on natural and experim..."
...…can be co-infected with S. mansoni and Schistosoma haematobium (Webster et al. 2012; Garba et al. 2013), their domestic livestock co-infected with S. bovis, S. curassoni and/or S. mattheei (Rollinson et al. 1990), and rodent wildlife co-infected with S. mansoni and S. rodhaini (Hanelt et al. 2010)....
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References
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TL;DR: Differences in infectivity, growth rates, maturation times, egg production and tissue deposition of eggs in the different strains of S. bovis are recorded.
Abstract: Summary Some biological characteristics of Schistosoma bovis Morocco, Sardinia and Iran in hamsters are described and discussed. Differences in infectivity, growth rates, maturation times, egg production and tissue deposition of eggs in the different strains are recorded. The egg shape and size of S. bovis Morocco, Sardinia, Iran, Kenya and S. mattheei are compared, as are the acid phosphatase, malate dehydrogenase and glucose 3-phosphate dehydrogenase isoenzymes. The compatibility/incompatibility of the same four strains of S. bovis to various members of the five species complexes of the genus Bulinus are recorded.
57 citations
TL;DR: Horizontal starch gel electrophoresis was used to score mobilities of seven different enzymes in species of Bulinus from North and West Africa and it was suggested that enzymic data should be used as taxonomic characters in parallel with morphological and anatomical characters.
Abstract: Horizontal starch gel electrophoresis was used to score mobilities of seven different enzymes in species of Bulinus from North and West Africa. An account of the intra- and inter-population variation observed was given. Based on the data obtained it was suggested that enzymic data should be used as taxonomic characters in parallel with morphological and anatomical characters. It is suggested that enzymic characters could be used to place taxa into synonymy if the data are collected in such a way that one can write up an enzyme profile for the single individual. The nine taxa of Bulinus known to occur in North and West Africa were revised, the taxon B. jousseaumei was synonymized with B. globosus, and the two taxa B. guernei and B. rohlfsi were synonymized with B. truncatus. As a result of the revision only six species could be recognized as valid from the area, these being B. forskalii, B. globosus, B. senegalensis, B. truncatus, B. ugandae and B. umbilicatus. Finally, some enzymic characters are suggested that may be used for a reliable identification of these morphologically very difficult taxa.
54 citations
Journal Article•
TL;DR: A snail survey in various parts of the Senegal River Basin, including the SenegalRiver Basin, temporary rain-fed pools, swamps, irrigation canals and drains, ricefields and Lac de Guier was carried out, finding Bulinus guernei was the most common, occurring in permanent habitats, and Bulinus senegalensis occurring in laterite pools in the eastern part of the Middle Valley.
Abstract: The results of four field surveys in Senegal are reported. 1. A snail survey in various parts of the Senegal River Basin, including the Senegal River, temporary rain-fed pools, swamps, irrigation canals and drains, ricefields and Lac de Guier was carried out. Three species of snails were commonly found: Bulinus guernei was the most common, occurring in permanent habitats, Bulinus senegalensis occurring in laterite pools in the eastern part of the Middle Valley, and also in the ricefields of Guede Chantier and Lampsar; B. forskalii was found in small numbers in Lac de Guier and Richard Toll. Three B. guernei were found to be naturally infected with S. bovis. Neither B. jousseaumei, B. globosus nor B. umbilicatus were found in our surveys. 2. A survey for urinary schistosomiasis was carried out in 100 villages (walo, near the Senegal River) and 11 villages (diere, away from the river) by delivering questionnaires in schools and by direct examinations of haematuria samples. The prevalence of haematuria varied between 0 and 33%. Generally, walos showed low rates of haematuria with the exception of Lampsar and Guede Chantier, and dieres showed higher rates of haematuria. 3. Examination of 400 cattle at the abattoir St. Louis, revealed a prevalence of 80% of schistosome infection. Two species were present, S. bovis and less commonly S. curassoni. Sometimes high worm burdens were seen, but lesions appeared to be minimal because of high ratio of male to female worms. 4. Examinations of 5722 sheep and 1752 goats in the abattoir, Dakar revealed an overall prevalence of 2.1%. Of the infected animals, 97.3% were infected with S. curassoni and 2.7% with S. curasonni and S. bovis. Laboratory snail infection experiments showed that S. curassoni is marginally compatible with B. senegalensis, but incompatible with B. guernei.
53 citations
TL;DR: It is concluded that any definite decision on the relative status of the two strains of S. intercalatum is still premature, in the light of what is known about other species of African Schistosoma.
Abstract: Seven enzyme systems [phosphoglucomutases (PGM), glucose phosphate isomerases (GPI), glucose-6-phosphate dehydrogenases (G6PD), malate dehydrogenases (MDH), laetate dehydrogenases (LDH), acid phosphatases (AcP) and hexokinases] in extracts of adult worms from two isolates of Schistosoma intercalatum , one from Zaire and one from Cameroun, were compared by isoelectric focusing. Two systems (GPI and PGM) were also compared in extracts of cercariae. Distinctive differences between the strains were found in the LDH system and even more marked differences in the G6PD and PGM systems (the latter were apparent in both adult worm and cercarial extracts). These observations are discussed in conjunction with existing evidence on the results of intermediate host infection experiments and of experimental hybridization between the two strains of S. intercalatum . In turn these aspects are discussed in the light of what is known about other species of African Schistosoma . It is concluded that any definite decision on the relative status of the two strains of S. intercalatum is still premature.
49 citations
TL;DR: It is finally concluded that the increasing water conservation and changing methods of husbandry may result in bovine schistosomiasis becoming a major veterinary problem in Africa.
Abstract: The present paper reviews the information available concerning the biology and transmission ecology of the African bovine species Schistosoma bovis, S. mattheei, S. margrebowiei and S. leiperi. Criteria for species identification (egg morphology, intermediate host spectra, definitive host-parasite relationships, etc.) are listed and the geographical distribution of the four species and factors determining the relative occurrence within their overall distributional ranges are described. S bovis and S. mattheei occur north and south of 10 degrees S, respectively, and S. margrebowiei occurs mainly, and S. leiperi only, in southern central Africa. Definitive host-related factors (susceptibility, water contact pattern, ect.) providing the background for being a primary definitive host and the primary definitive host spectra for the four schistosome species are described. The primary definitive host spectrum for S. margrebowiei and S. leiperi comprise lechwe, puku and waterbuck, for S. mattheei lechwe, puku, waterbuck plus cattle, and for S. bovis cattle and possibly also some of the listed antelope species. In addition, wild bovines and cattle may provide a reservoir of S. mattheei and S. margrebowiei in humans, but wild bovines and domestic stock play no major role in the transmission of other human species of schistosomes. The intermediate snail host spectra of S. mattheei and S. leiperi only comprise members of the Bulinus africanus species complex; S. bovis is transmitted by members of the B. truncatus, B. africanus and B. forskalii species groups, and S. margrebowiei is transmitted by members of the B. forskalii species group and possibly also by members of the B. tropicus and B. truncatus species groups. Factors determining the transmission ecology of the four schistosome species, and thereby the epidemiology of bovine schistosomiasis, are discussed. Influential factors comprise environmental conditions mediated via the effect of these on the size of the snail host population and on the rate of the intramolluscan development, behavioural patterns of the definitive host population and the course of the infection in the definitive host as related to aspects of susceptibility and level of endemicity. The epidemiological pattern (prevalence and intensity of infection, seasonality of transmission, etc.) is described and exemplified, and it is finally concluded that the increasing water conservation and changing methods of husbandry may result in bovine schistosomiasis becoming a major veterinary problem in Africa.
46 citations