Multi-parasite host susceptibility and multi-host parasite infectivity: a new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism.

In this study, we analyze the degree of susceptibility/un-susceptibility of five strains of Biomphalaria glabrata from different geographical origins successively challenged with a panel of 4 Schistosoma mansoni strains. A total of 20 homopatric and heteropatric host-parasite combinations were tested with exposure doses of 1, 10, 20, 30 and 50 miracidia per individual host. By doing this, we characterized each B. glabrata strain by its "multi-parasite susceptibility phenotype" that reflects better the efficiency of their defense mechanism against not only one, but a diversity of schistosome stocks. In the same time, all the S. mansoni strains used were characterized, by their "multi-host infectivity phenotype" that reflects the level of infectivity they display when confronted to diverse snail populations. Based on these results it is possible to select different homogenous stocks of snails with different spectrum of susceptibility/un-susceptibility for several parasite strains. This will be a useful tool for future functional studies conducted to understand the genetics and molecular basis of the compatibility polymorphism in this host/parasite model.

Effects of laboratory culture on compatibility between snails and schistosomes.

The genetic control of compatibility between laboratory strains of schistosomes and their snail hosts has been studied intensively since the 1970s. These studies show (1) a bewildering array of genotype-by-genotype interactions - compatibility between one pair of strains rarely predicts compatibility with other strains, and (2) evidence for a variety of (sometimes conflicting) genetic mechanisms. Why do we observe such variable and conflicting results? One possibility is that it is partly an artifact of the use of laboratory strains that have been in culture for many years and are often inbred. Here we show that results of compatibility trials between snails and schistosomes - all derived from the same natural population - depend very much on whether one uses laboratory-cultured or field-collected individuals. Explanations include environmental effects of the lab on either host or parasite, and genetic changes in either host or parasite during laboratory culture. One intriguing possibility is that genetic bottlenecks during laboratory culture cause the random fixation of alleles at highly polymorphic loci that control the matched/mismatched status of hosts and parasites. We show that a simple model of phenotype matching could produce dose response curves that look very similar to empirical observations. Such a model would explain much of the genotype-by-genotype interaction in compatibility observed among strains.

Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation.

We investigated local adaptation in the spatially structured natural Biomphalaria glabrata/Schistosoma mansoni host-parasite system in the marshy forest focus of Guadeloupe using cross-transplantation experiments. We demonstrated strong and highly significant variations in susceptibility/infectivity of host and parasite populations, respectively, but found no evidence of local adaptation neither for S. mansoni nor for B. glabrata. Environmental as well as genetic factors are discussed to explain susceptibility/infectivity variations between both host and parasite populations. The absence of local adaptation is discussed in relation to the metapopulation dynamics of both host and parasite, in particular their relative rates of dispersal at the scale under scrutiny. Our study constitutes the first cross-transplantation experiment concerning this host-parasite system of which both hosts and parasites came directly from the wild, excluding laboratory generations and experimental host passages.

Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni.

Snail immune responses towards a trematode infection are known to rely on both plasmatic and cellular host factors. As an approach to further investigate the suspected involvement of plasmatic factors in Biomphalaria glabrata resistance/susceptibility to Echinostoma caproni, we compared protein patterns of plasma collected from susceptible and resistant snails. This proteomic approach revealed that 13 plasmatic proteins exhibited significant differences in their apparent representativity. The genes corresponding to five of them were characterised by a combination of mass spectrometry and molecular cloning. They encode two isoforms of a glycolytic enzyme, two isoforms of a calcium binding protein and an inhibitor of cysteine protease. Furthermore, we investigated gene expression in parasite-exposed or -unexposed snails as well as in various tissues by quantitative PCR. This study showed that: (i) differential representation of plasma proteins between the snail strains was correlated with a differential level of transcripts; (ii) expression of these genes after parasite exposure was differentially regulated in the two strains; and (iii) these genes were expressed predominantly in the albumen gland.

Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts.

We investigated the genotypic composition of the digenetic parasite Schistosoma mansoni for its adult stages within the definitive host (the wild rat, Rattus rattus) and for the larval stages within the intermediate host (the snail, Biomphalaria glabrata) both collected at the same transmission site. Our analyses are based upon the recognition and distribution of 200 different multilocus genotypes generated by RAPD markers. While intramolluscan larval infrapopulations are characterized by a low infection rate (0.6 % on average) and low intra-host genetic diversity (1.1 genotype on average per infected snail), adult infrapopulations within rats showed a high infection rate (94%) and a substantial intra-host genetic diversity (34 genotypes on average) linked to high intensities (160 worms per host on average). A single definitive host bearing 105 different genotypes harboured 52 % of the total genetic diversity detected within the whole parasite population. Analysis of the genetic data allowed the identification of various ecological, behavioural and immunological factors which are likely to enhance transmission of multiple parasite genotypes towards the vertebrate hosts. From the distribution of repeated identical multilocus genotypes within the parasite population and among the hosts, we have inferred different parameters of the cercarial transmission efficiency as well as patterns and processes by which vertebrate hosts acquire infection in the field.

Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism?

Failure of snail reinfection by Schistosoma mansoni has been demonstrated in susceptible Biomphalaria glabrata infected with 1 miracidium and subsequently re-exposed to 1 or 5 homologous parasite larvae. The acquisition of 'resistance' to secondary parasite infection was time dependent since complete inhibition was observed at 2 weeks and longer following monomiracidial exposure. This phenomenon was still observed in snails challenged 8 weeks after primary infection. Histological observations revealed that sporocysts from the challenge infection were free of encapsulation, their development was stopped and they degenerated slowly in the absence of haemocytic reaction of the host. Under the hypothesis of an acquired homologous resistance mechanism, this strongly suggests that 1 or several unidentified humoral factors are responsible for the non-development of the sporocysts from the challenge infection. However, considering the time-dependent nature of the phenomenon, an intraspecific larval antagonism process between sporocysts resulting from the primary infection and those from the challenge infection may be involved.

Host choice by larval parasites: a study of Biomphalaria glabrata snails and Schistosoma mansoni miracidia related to host size.

Within snail/trematode associations the age/size of the host at infection has consequences with regard to miracidial infection success, further intramolluscan parasite development and reproduction, and the host response, mainly in terms of growth and reproductive effort. Taking into account these differences, we were interested in determining whether miracidia could discriminate and make a choice between snails of different sizes. Using the Schistosoma mansoni/Biomphalaria glabrata system, we compared data on the snail infection rate and the mother sporocyst abundance among three size classes of snails (juvenile, subadult, and adult) exposed separately or together to the parasite larvae. When exposed individually, juvenile snails (3-5 mm) had significantly higher prevalence and abundance values than did subadult snails, followed by adult snails. In contrast, when snails of the three size classes were exposed together in heterogeneous size groups the prevalence and abundance values were always significantly higher for subadult snails of the 7- to 9-mm class than for juvenile and adult snails. A host choice experiment confirmed that significantly more miracidia were attracted by subadult snails, suggesting that the parasite has been selected for specific locating and recognition mechanisms increasing the infection rate of subadult snails when the latter have been exposed in a heterogeneous size group. Selective forces that may be responsible for such a preferential infectivity of the parasite vis-à-vis particular host age/size class are discussed in relation to host resources and host responses.

Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes.

Parasite prevalences, miracidia developmental capacity, mother sporocyst mean intensities, sporocyst distribution patterns, and cercarial production levels were determined after individual exposure of Biomphalaria glabrata snails to increased doses of Schistosoma mansoni miracidia for two geographical strains (Brazilian, BRE, and Guadeloupean, GUA) of host and parasite. For a high level (100%) of host-parasite susceptibility and in the absence of mother sporocyst regulatory processes for the BRE combination, parasites were randomly dispersed among snail hosts with a frequency distribution conforming to a positive binomial. In contrast, for a moderate level (65%) of host-parasite susceptibility and in the presence of mother sporocyst regulatory processes for the GUA combination, parasites were overdispersed among snail hosts with a frequency distribution conforming to the negative binomial. Levels of cercarial production were found to be strain dependent, to be determined during early development of mother sporocysts, and to be correlated with the number of developed mother sporocysts. Results were analyzed in the general context of the infrapopulation dynamics of the intramolluscan stages of trematode and are discussed in terms of their consequences on the distribution of the genetic diversity of adult schistosomes among the definitive host population.