Schistosoma haematobium, S. intercalatum, S. japonicum, S. mansoni, and S. rodhaini in mice: relationship between patterns of lung migration by schistosomula and perfusion recovery of adult worms.

The development of five schistosome species was compared in mice by the recovery of schistosomula from chopped lung tissue and of adult worms by portal perfusion. Three developmental patterns appeared. (1) Schistosoma japonicum was unique in showing an early establishment of schistosomula in and a rapid departure from the lungs together with the highest worm recovery; (2) S. haematobium contrasted by establishing later and persisting in the lungs for at least 2 weeks while yielding the lowest adult worm recovery; and (3) S. intercalatum, S. mansoni, and S. rodhaini had an intermediate pattern--they resided in the lungs for several days, then disappeared and produced intermediate numbers of adults. Lung petechiae, known to accompany the migration of S. japonicum, were never detected after infection with the other species. We speculate that the three migration patterns of schistosomes are related to the size of the relative spectra of naturally infected definitive hosts.

Schistosome-induced portacaval haemodynamic changes in Rattus rattus are associated with translocation of adult worms to the lungs.

The presence of naturally portacaval shunts has been investigated in the vasculature of normal and Schistosoma mansoni-infected Rattus rattus. Using the technique of injecting Polystyrene microspheres in the superior mesenteric vein, we demonstrated that the presence of adult schistosomes in the lungs of R. rattus was not due to an innate anomaly of the rat vasculature but resulted from the formation of portacaval shunts during infection. In rats harbouring a bisexual infection, microspheres were only detected in the lungs from week 7. The development and increasing size of the shunts were maximal between weeks 7 and 10 and coincident with the translocation of adult worms from the portal tract to the lungs. At weeks 20-25, only 1-2% of the microspheres were recovered from the lungs, suggesting that the portacaval anastomoses have regressed due to reduction in portal hypertension after worm translocation. R. rattus with a male-only schistosome infection harboured adult worms in the lungs, indicating that the development of shunts does not solely depend upon egg deposition in the liver to generate hypertension. The relationships between the presence of the schistosomes in the lungs, the portacaval shunting and the resistance to reinfection is discussed.

Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali.

Random amplified polymorphic DNA (RAPD) markers were used to assess distribution and genetic diversity of Schistosoma haematobium populations within their bulinid intermediate hosts in Mali. Naturally infected snails (Bulinus truncatus and B. globosus) were collected at four sites in the Bamako district. S. haematobium cercariae from single snails were used to infect mice and genotypes of the resultant adult worms were characterized using RAPD markers. Diversity indices were calculated at the scale of one snail, both within and among sites. One third of the molluscs harboured multiple miracidial infections (the maximum number equal to five) with slightly overdispersed distributions in three sites and a random distribution at one site. Similarity indices revealed significantly less variation among populations compared with populations, indicative of the absence of distinct S. haematobium populations within the Bamako district. RAPD markers represent an accurate tool for determining genetic diversity and amount of gene flow among parasite populations contained within different individual snails and among intermediate host populations.

Permissiveness of two African wild rodents, Mastomys huberti and Arvicanthis niloticus, to Schistosoma intercalatum: epidemiological consequences.

The compatibility between Schistosoma intercalatum (Cameroon) and two wild rodents commonly found in Africa. Mastomys huberti (the multimammate mouse) and Arvicanthis niloticus (the Nile rat) was studied to determine their biological capacities to act as hosts for S. intercalatum. In both rodent species the general mean worm recovery was high (33 +/- 0.1% in M. huberti and 33.8 +/- 0.1% in A. niloticus) and worm mortality was very low from 6 to 20 weeks postinfection; parasite maturity was reached. The high number of released eggs as well as the viability and the infectivity of the miracidia to the snail vector showed that M. huberti and A. niloticus are very permissive to S. intercalatum and may act as hosts for the human disease.

Competitive exclusion in human schistosomes: the restricted distribution of Schistosoma intercalatum.

A study on the immune and mating interactions between Schistosoma intercalatum and S. mansoni has been carried out. The immunologically mediated interactions and mating patterns observed between the two species demonstrate that S. mansoni is competitively dominant over S. intercalatum. When S. mansoni females are absent, S. mansoni males are more competitive than S. intercalatum males at pairing with S. intercalatum females. The use of a mathematical model shows how the abundance of S. mansoni worms per host could dramatically affect the mating probability of S. intercalatum females with their homologous males. It appears that the competitive exclusion between these two species of schistosomes may probably be an important factor restricting the distribution of S. intercalatum in Africa.

ITS2 ribosomal RNA indicates Schistosoma hippopotami is a distinct species.

The internal transcribed spacer region of the ribosomal RNA, ITS2, was sequenced from a single specimen of S. hippopotami collected from a pulmonary artery of the hippopotamus, Hippopotamus amphibius in South Africa. The nucleotide sequence was aligned with those of S. mansoni, S. rodhaini, S. haematobium, S. intercalatum, S. curassoni, S. bovis and S. japonicum. Both maximum parsimony and genetic distance analyses were performed on these data sets. Using S. japonicum as outgroup to the African schistosomes, a single most-parasmonious tree was obtained of length 64 steps with a consistency index of 1-S. hippopotami was the sister-group to the remaining African species. This species has lateral-spined eggs and its basal position in the tree suggests that this condition is primitive and that terminal-spined eggs developed secondarily. Molecular data clearly show that S. hippopotami cannot be considered synonymous with S. mansoni. Assuming the hippopotamus is the normal host of S. hippopotami, phylogenetic analysis is consistent with an ancient association between schistosomes and ungulates.

Parthenogenesis in schistosomatidae.

Among which species, in what situations and how, does parthenogenesis occur in the biology of reproduction of schistosomes? Here, José Jourdane, Daniéle Imbert-Establet and Louis Albert Tchuem Tchuenté review the literature on parthenogenesis in schistosomes, and debate the evolutionary aspects of this type of reproduction.

Change of mate and mating competition between males of Schistosoma intercalatum and S. mansoni.

Previous studies on mating behaviour of Schistosoma intercalatum and S. mansoni, two human schistosomes which may overlap in parts of Africa, have shown that in mixed infections in mice there are no physiological barriers preventing heterospecific pairings. However, when choice is possible, matings occur preferentially between partners of the same species. In this paper, further experimental studies on mating behaviour of the two species were conducted. Sequential infections showed that heterospecific pairs of worms change partners to homospecific pairs when given the opportunity. The change of mate is a progressive process requiring up to, at least 8 weeks, and this phenomenon is due to the male worm seeking the appropriate female. S. mansoni males are better at pairing with females than S. intercalatum males, and they will change partner to pair with homologous females in preference to heterologous females whenever given the opportunity. Moreover, in the absence of S. mansoni female worms, unpaired S. mansoni male worms pull away female S. intercalatum from male S. intercalatum. It appears from this study that S. mansoni males are much more competitive than S. intercalatum males at pairing with females, and this is a disadvantage for S. intercalatum in situations of sympatry.

Interspecific stimulation of parthenogenesis in Schistosoma intercalatum and S. mansoni.

Experimental studies of mating behaviour of Schistosoma intercalatum and Schistosoma mansoni in mixed infections in mice showed that in simultaneous infections, without the possibility of choice of mate, heterologous pairing occurs readily. The paired females reach sexual maturity, are inseminated and lay parthenogenetic eggs. Miracidia originating from the S. mansoni male x S. intercalatum female are non infective to either Biomphalaria glabrata or Bulinus forskalii, whereas those from the reverse cross show a very low infectivity to only B. glabrata. The resulting haploid male cercariae also show a very low infectivity to mice (1.1%) and consequently only a very small number of adult worms develop. It appears from this study, on chromosomal and electrophoretic evidence, that generative (haploid) parthenogenesis occurs in S. mansoni females paired with S. intercalatum males.

Parthenogenesis in the genus Schistosoma: electrophoretic evidence for this reproduction system in S. japonicum and S. mansoni.

Mixed infections with Schistosoma japonicum and S. mansoni were carried out in mice. S. japonicum females paired with S. mansoni males developed normally and produced numerous viable eggs; very little sperm was found in the female genital tract. The eggs yielded many miracidia infective to Oncomelania hupensis, the host of S. japonicum. Cercariae arising from miracidia developed into male worms with an electrophoretic pattern of malate dehydrogenase (MDH) corresponding only to the maternal species S. japonicum. S. mansoni females paired with S. japonicum produced few viable eggs; sperm was found in the female genital tract. Miracidia hatched from some of these eggs were infective to Biomphalaria glabrata, the host of S. mansoni. Cercariae arising from miracidia developed into female worms with an electrophoretic pattern of MDH typical of the maternal species S. mansoni. It was concluded that S. japonicum females paired with S. japonicum males reproduce parthenogenetically. Parthenogenesis in schistosomes is discussed.

Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America.

Mitochondrial DNA was analyzed from 6 strains of Schistosoma mansoni with 12 restriction enzymes, corresponding to 40 restriction sites or about 1.5% of the coding region. An extensive length polymorphism among strains of S. mansoni was found, with size ranging from 16,500 bp to 24,900 bp. Five restriction sites among 40 were polymorphic; phylogenetic analysis using parsimony criteria supports the idea that American strains were introduced very recently from Africa. Two large fragments (2800 and 5400 bp), representing half of the coding region were cloned. The location of some genes was determined using heterospecific multigenes probes and suggests that this platyhelminth genome differs from all other known mtDNA gene organization.

Genetic variability and evolution of the Schistosoma genome analysed by using random amplified polymorphic DNA markers.

The usefulness of random amplified polymorphic DNA markers (RAPD) was assayed in an attempt to discriminate among species, strains and individuals within the genus Schistosoma. Depending on the species, 40-50 arbitrary decamer oligonucleotides were used as primers to amplify total DNA by the polymerase chain reaction (PCR). An important polymorphism was observed among 5 species, allowing a phylogenetic tree to be outlined. These differences can be used for rapid and accurate identification. A limited but easily detectable polymorphism was revealed among 3 strains of a single species (Schistosoma mansoni). Minor differences were observed among individuals of a single strain. A RAPD marker allows sexual discrimination between individuals from the terminal spined-egg species group. Although a limited number of strains have been examined, the results already indicate clearly that RAPD markers constitute a powerful tool for the analysis of genetic variability. This new tool will considerably extend the information available from morphology, isozyme and limited restriction fragment length polymorphism data and opens the way to genetic analysis of these species.

Choice of mate, a reproductive isolating mechanism between Schistosoma intercalatum and S. mansoni in mixed infections.

In Africa, the two human schistosome parasites, Schistosoma intercalatum and S. mansoni, can be found sympatrically, which poses the problem of the nature of their reproductive isolation. In this paper, experimental studies of mating behaviour in mixed infections in mice were carried out. Simultaneous infections without choice of mate showed an absence of any physiological barriers preventing encounter and mating of the two species on the same host. Whenever choice was possible, mating did not occur in a random way, but preferentially between partners of the same species (there was a significant prevalence of homospecific pairs). S. mansoni exhibited greater specific mate recognition than S. intercalatum. Moreover, in the absence of S. mansoni female worms, S. mansoni male worms were as competitive as S. intercalatum male worms in pairing with S. intercalatum female worms. It appears from this study that the choice of mate is a reproductive isolating factor between the two species.

Molecular evidence linking hominid evolution to recent radiation of schistosomes (Platyhelminthes: Trematoda).

Molecular phylogenies for seven species of schistosomes, including four species infecting man, were constructed from PCR-amplified sequences of two ribosomal genes: one nuclear (internal transcribed spacer 2 in the ribosomal multigenic family) and one mitochondrial (16S rDNA). The two phylogenies obtained are congruent, and the data suggest that the mitochondrial sequence evolves about three times faster than the nuclear sequence. We propose a calibration of the phylogenetic tree of schistosomes that dates "human capture" of these parasites from other animal hosts (rodents and ruminants) in Africa to 1-10 million years ago, when the first hominids invaded savanna areas, which are the favorable environment for parasite transmission.

Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment.

Dynamics of natural populations of Schistosoma mansoni were studied during 8 consecutive years among Rattus rattus populations from 8 transmission sites of the marshy forest focus of Guadeloupe (French West Indies). The schistosome population is over-dispersed (k = 0.119) within the murine hosts and ecological factors linked to the patchy environment may be responsible for such aggregated distribution. Analysis of the spatio-temporal variations in prevalences, intensities and abundances showed limited variations of the infection during the 8 years at the level of the whole parasite population but great spatial heterogeneity at the level of local schistosome populations. Inter-populational genetic variability linked to the degree of adaptation of this human parasite to the murine host may explain differences in transmission dynamics between the local populations of S. mansoni.

The mouse as a suitable host for an isolate of Schistosoma haematobium from Niger.

The host-parasite relationships of a Schistosoma haematobium isolate, originating from Niger, and the white mouse are described. Swiss OF1 albino mice were exposed individually to 200 cercariae and worms were recovered 9, 12, 16 and 20 weeks post infection. The mean worm returns ranged between 10.54 and 13.05% and did not alter significantly between 9 and 20 weeks post infection. The sex ratio of worms was always in favour of males; from 7.09:1 at 9 weeks after infection it decreased regularly to 3.28:1 at 20 weeks. Male worms reached a mean length of 8.72 mm at 20 weeks. From the 12th week post infection, a high number of eggs was found in the liver and gut. At 20 weeks, eggs were also found in the bladder. Viable eggs and infective miracidia were obtained. The infection of Bulinus truncatus from Niger succeeded with a mean rate of 61% after the first passage through mice. The isolate of S. haematobium was maintained in the laboratory during 3 successive passages through mice. These entirely new results are very probably linked to genetic characteristics peculiar to the S. haematobium populations from Niger.

Relocation of Schistosoma mansoni in the lungs and resistance to reinfection in Rattus rattus.

The localization of adult Schistosoma mansoni originating from Guadeloupe (West Indies) was analysed in the natural host Rattus rattus in experimental and natural infections. A transfer of schistosomes from the porto-mesenteric system to the lungs occurs between the 4th and the 20th weeks post-infection, with a peak between 4 and 8 weeks; it should be noted that the worms start laying eggs at 4 weeks post-infection. In both experimentally and naturally infected R. rattus the relocation of schistosomes in the lungs is correlated with the total worm burden. Between 6 and 12 weeks post-infection some adult worms and numerous eggs are trapped in the liver. A high mortality in the worm population coincides with the migration of the parasites from the porto-mesenteric veins to the lungs. In re-infected R. rattus a relationship appears between the presence of schistosomes in the lungs and resistance to reinfection. It is concluded that, as already postulated previously in mice, resistance to re-infection in the natural host R. rattus is at least partly correlated with the hepatic pathology caused by the schistosomes of the primary infection.

Influence of intramolluscan larval stages of Echinostoma liei on the infectivity of Schistosoma mansoni cercariae.

During co-infection of Biomphalaria glabrata with Schistosoma mansoni and Echinostoma liei, S. mansoni cercariae released before the complete resorption of S. mansoni sporocysts show a very strong decrease of their infectivity in mice. Under conditions of high interspecific competition (i.e. when the snails are infected by E. liei 8 days after infection by S. mansoni), the mean overall worm return is five times lower than that of the control experiment. A marked decrease of the infectivity of cercariae is also noted when snails, infected exclusively with either sporocysts of S. mansoni or rediae of E. liei, are associated in the same tank.