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.

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Bidirectional introgressive hybridization between a cattle and human schistosome species.

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.

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

Available data in the literature pertaining to the life-history characteristics of all known species of mammalian schistosomes have been gathered, and correlations between such variables as length of pre-patent period, adult worm size, rate of progeny production and progeny size have been explored. Accommodation of the schistosome life-cycle to the constraints imposed by certain host characteristics such as life-expectancy and size is discussed. Of the 23 known species of mammalian schistosomes, 20 species apparently rely to a major extent on relatively large-bodied and long-lived mammals such as primates, ungulates and proboscideans for their transmission. Only 1 species, Schistosomatium douthitti, is exclusively dependent on rodents for its transmission. S. douthitti attains maturity within its definitive host faster than any other mammalian schistosome, and is the only species known to be capable of producing viable eggs by facultative parthenogenesis. For all species of mammalian schistosomes, adult worm size, as estimated by female length, is positively correlated with the number of uterine eggs contained within the female (r = 0·682). For the 7 species for which data exist, rate of egg production/worm pair/day is positively correlated with uterine egg counts (r = 0·873) and inversely correlated with egg length (r = −0·787) and miracidium length (r = −0·953). Length of the pre-patent period is positively correlated with egg length (r = 0·503). With respect to the molluscan host, the number of cercariae produced by snails is positively correlated with the shell size of the snail (r = 0·657). For the 5 species for which data exist, the rate of egg production is inversely correlated with shell size of the intermediate host (r = −0·955) and the common logarithm of the number of cercariae produced (r = −0·893). Comparisons between species suggest that exceptionally low rates of cercariae production in the intermediate host may be compensated for by rapid rates of egg production in the definitive host, implying a degree of integration in the schistosome life-cycle not previously appreciated. Most species of mammalian schistosomes have long-lived definitive hosts, and snail hosts capable of producing many cercariae; compensatory relationships are therefore less obvious in such species. Additional quantitative data on all aspects of schistosome life-histories, particularly rate and duration of egg production, are needed to confirm or refute the relationships discussed above.

A comparative study of the life-histories of mammalian schistosomes.

Characterizing host and parasite population genetic structure and estimating gene flow among populations is essential for understanding coevolutionary interactions between hosts and parasites. We examined the population genetic structure of the trematode Schistosoma mansoni and its two host species (the definitive host Rattus rattus and the intermediate host Biomphalaria glabrata) using microsatellite markers. Parasites were sampled from rats. The study was conducted in five sites of the Guadeloupe Island, Lesser Antilles. Mollusks display a pattern of isolation by distance whereas such a pattern is not found neither in schistosomes nor in rats. The comparison of the distribution of genetic variability in S. mansoni and its two host species strongly suggests that migration of parasites is principally determined by that of the vertebrate host in the marshy focus of Guadeloupe. However, the comparison between genetic differentiation values in schistosomes and rats suggests that the efficacy of the schistosome rat-mediated dispersal between transmission sites is lower than expected given the prevalence, parasitic load and migration rate of rats among sites. This could notably suggest that rat migration rate could be negatively correlated to the age or the infection status of individuals. Models made about the evolution of local adaptation in function of the dispersal rates of hosts and parasites suggest that rats and mollusks should be locally adapted to their parasites.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.0014-3820.2005.tb00990.x

Dispersal in a parasitic worm and its two hosts: consequence for local adaptation

In Guatemalan villages people commonly rear pigs, and both hosts may be infected with Ascaris. This study was designed to ask whether both humans and pigs are potential hosts in a single parasite transmission cycle in such villages, or alternatively, if there are two separate transmission cycles, one involving pigs and one involving human hosts. Parasites were collected from both host species from locations in the north and south of Guatemala. Allelic variation in the nuclear genome of Ascaris was measured using enzyme electrophoresis, while mitochondrial DNA (mtDNA) sequence variation was quantified using restriction mapping. Low levels of enzyme polymorphism were found in Ascaris, but allele frequencies at two loci, mannose phosphate isomerase and esterase, suggest that there is little gene exchange between parasite populations from humans and pigs. MtDNA haplotypes fall into two distinct clusters which differ in sequence by 3-4%; the two clusters broadly correspond to worms collected from humans and those collected from pigs. However, some parasites collected from humans have mtDNA characteristic of the 'pig Ascaris' haplotype cluster, while some parasites collected from pigs have mtDNA characteristic of the 'human Ascaris' haplotype cluster. These shared haplotypes are unlikely to represent contemporary cross-infection events. Patterns of phylogenetic similarity and geographical distribution of these haplotypes suggest, instead, that they are the result of two historical introgressions of mtDNA between the two host-associated Ascaris populations. The results clearly demonstrate that Ascaris from humans and pigs are involved in separate transmission cycles in Guatemala.

Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala.

Summary Experiments were designed to examine the mating behaviour of Schistosoma haematobium and S. intercalatum in mixed infections in hamsters. Individual worms were identified by electrophoretic analysis of glucose-6-phosphate dehydrogenase which was characteristic for each isolate, in addition the uterine eggs of individual females were examined. The results showed that a specific mate recognition system does not exist for S. haematobium and S. intercalatum. The application of statistical tests to the results suggests that S. haematobium male worms are better at pairing with female worms of either species than S. intercalatum male worms. The significance of the results is discussed in relation to an occurrence of natural hybridization between these species in Cameroun.

Mating behaviour in mixed infections of Schistosoma haematobium and S. intercalatum

A comparative study on the development of Senegalese isolates of Schistosoma curassoni, S. haematobium and S. bovis in hamsters is reported, together with the compatibility of these parasites with Bulinus spp. and enzymes of adult worms. The mean worm return from 35 hamsters exposed to 100 cercariae each of S. curassoni was 11·5%, and of these 54% were paired, the remainder were single males. The growth and maturation of the worms were recorded from 40 to 100 days. The cross-over point (when paired females are of the same length as paired males) was reached at 42 days post-infection when the worms averaged 13·7 mm in length. The majority of tissue eggs (84·5%) were recovered from the liver, compared with 11% in the colon, 2·5% in the caecum and 1·6% in the small intestine. Estimates of the fecundity of paired females averaged 167 eggs/day per female worm. Snail-infection experiments showed S. curassoni to be compatible with B. umbilicatus, marginally compatible with B. senegalensis and incompatible with B...

On Schistosoma curassoni, S. haematobium and S. bovis from Senegal: development in Mesocricetus auratus, compatibility with species of Bulinus and their enzymes

An enzymatic comparison has been made between isolates of Schistosoma mansoni from rats and humans in Guadeloupe and a Burundi isolate of S. rodhaini . Analyses of LDH, MDH, AcP, PGM, GPI, G6PDH and HK by isoelectric focusing provided no evidence for the involvement of S. rodhaini in the recent evolution of the schistosomes currently endemic in Guadeloupe. No distinction could be made between murine and human isolates of S. mansoni and it is suggested that murine schistosomiasis should not therefore be ignored in control programmes. Rattus rattus were captured at seven sites around the island; of 142 examined, 48 were positive for schistosomes. Differences in prevalence between habitats were marked and only small changes in prevalence were observed in localities sampled in 1982 and 1983. Animals with the greatest worm burdens were associated with areas of high prevalence, and age-related changes in worm burden were observed. Two alleles, a and b , at the MDH-1 locus of S. mansoni from rats were identified. Differences in the overall frequencies of these alleles were observed for schistosomes from different localities. Allelic frequences representative of schistosomes from rats at four localities were stable from 1982 to 1983. The majority of positive animals, even those with light worm burdens, were found to be infected with a number of different schistosome genotypes.

Schistosoma mansoni from naturally infected Rattus rattus in Guadeloupe: identification, prevalence and enzyme polymorphism.

The eggs ofSchistosoma bovis isolated from Misungwi, Tanzania measure 211.1 μm±18.4 long and 66.7 μm±5.4 wide. The parasite is naturally transmitted byBulinus africanus and is compatible in the laboratory with snails belonging to theB. truncatus, B. forskali, andB. reticulatus groups. The compatibility withB. africanus group snails is shared with isolates from Kenya and Sudan but not withS. bovis from more northern distributions. Enzyme analyses were carried out by isoelectric focusing. In adult worms, phosphoglucomutase (PGM), hexokinase (HK), malate dehydrogenase (MDH), and lactate dehydrogenase (LDH) proved to be monomorphic whereas two types of glucosephosphate isomerase (GPI), three types of glucose-6-phosphate dehydrogenase (G6PDH), and two types of acid phosphatase (AcP) were identified. Differences in the pI values of GPI and MDH of snail digestive glands and of larval parasites allowed the intramolluscan stages to be characterised. The GPI heterogeneity encountered was common both to the larval and adult parasites. The enzyme types identified inS. bovis are discussed both from an intra- and interspecific viewpoint.

Observations on an isolate of Schistosoma bovis from Tanzania.

There are two main and two weak fractions of malate dehydrogenase isoenzyme common toSchistosoma bovis, S. leiperi, S. margrebowiei andS. mattheei: a major fraction at pI 8.56, seconded at pI 7.38, with weaker activity at pI 7.05 and pI 8.15. Variation in malate dehydrogenase occurs in some species/strainsen passage.

G. C. Ross

Papers

Mating behaviour in mixed infections of Schistosoma haematobium and S. intercalatum

On Schistosoma curassoni, S. haematobium and S. bovis from Senegal: development in Mesocricetus auratus, compatibility with species of Bulinus and their enzymes

Schistosoma mansoni from naturally infected Rattus rattus in Guadeloupe: identification, prevalence and enzyme polymorphism.

Observations on an isolate of Schistosoma bovis from Tanzania.

Observations on some isoenzymes of strains of Schistosoma bovis; S. mattheei, S. margrebowiei, and S. leiperi.