André Théron

Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes.

Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission. Almost all cercariae are free-living in the external environment. With a few exceptions (cercariae of Halipegus occidualis (Halipegidae) can live several months, Shostak & Esch, 1990a), cercariae have a short active life during which they do not feed, living on accumulated reserves. Most cercariae encyst as metacercariae in second intermediate hosts which are prey of the definitive host; in certain species, the interruption of the active life is achieved by an encystment in the external environment (or a simple immobile waiting strategy in a few species). In some two-host life cycles, the cercariae develop into adults after penetration (this is the case for various species causing human schistosomiasis). Some cercariae do not leave the mollusc which must then be ingested by the definitive host.

DISPERSAL IN A PARASITIC WORM AND ITS TWO HOSTS: CONSEQUENCE FOR LOCAL ADAPTATION

Abstract 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.

Origin and diversification of the human parasite Schistosoma mansoni

Schistosoma mansoni is the most widespread of the human‐infecting schistosomes, present in 54 countries, predominantly in Africa, but also in Madagascar, the Arabian Peninsula, and the Neotropics. Adult‐stage parasites that infect humans are also occasionally recovered from baboons, rodents, and other mammals. Larval stages of the parasite are dependent upon certain species of freshwater snails in the genus Biomphalaria, which largely determine the parasites geographical range. How S. mansoni genetic diversity is distributed geographically and among isolates using different hosts has never been examined with DNA sequence data. Here we describe the global phylogeography of S. mansoni using more than 2500 bp of mitochondrial DNA (mtDNA) from 143 parasites collected in 53 geographically widespread localities. Considerable within‐species mtDNA diversity was found, with 85 unique haplotypes grouping into five distinct lineages. Geographical separation, and not host use, appears to be the most important factor in the diversification of the parasite. East African specimens showed a remarkable amount of variation, comprising three clades and basal members of a fourth, strongly suggesting an East African origin for the parasite 0.30–0.43 million years ago, a time frame that follows the arrival of its snail host. Less but still substantial variation was found in the rest of Africa. A recent colonization of the New World is supported by finding only seven closely related New World haplotypes which have West African affinities. All Brazilian isolates have nearly identical mtDNA haplotypes, suggesting a founder effect from the establishment and spread of the parasite in this large country.

Genetic structure in natural populations of flukes and snails: a practical approach and review

Several aspects of the coevolutionary dynamics in host-parasite systems may be better quantified based on analyses of population structure using neutral genetic markers. This includes, for example, the migration rates of hosts and parasites. In this respect, the current situation, especially in fluke-snail systems is unsatisfactory, since basic population genetics data are lacking and the appropriate methodology has rarely been used. After reviewing the forces acting on population structure (e.g. genetic drift or the mating system) and how they can be analysed in models of structured populations, we propose a simplified, indicative framework for conducting analyses of population structure in hosts and parasites. This includes consideration of markers, sampling, data analysis, comparison of structure in hosts and parasites and use of external data (e.g. from population dynamics). We then focus on flukes and snails, highlighting important biological traits with regard to population structure. The few available studies indicate that asexual amplification of flukes within snails strongly influences adult flukes populations. They also show that the genetic structure among populations in strongly affected by traits in other than snails (e.g. definitive host dispersal behaviour), as snails populations have limited migration. Finally more studies would allow us to deepen our current understanding of selective interference between flukes and snails (e.g. manipulation of host mating system by parasites), and evaluate how this affect population structure at neutral markers.

GENETIC DIVERSITY AND RECRUITMENT PATTERN OF SCHISTOSOMA MANSONI IN A BIOMPHALARIA GLABRATA SNAIL POPULATION: A FIELD STUDY USING RANDOM-AMPLIFIED POLYMORPHIC DNA MARKERS

Random-amplified polymorphic DNA markers have been used to assess the amount and the distribution of the genetic diversity of Schistosoma mansoni within a natural population of Biomphalaria glabrata at a transmission site of the murine schistosomiasis focus of Guadeloupe. Despite high infection rate and heavy schistosome load within the definitive hosts (Ratus rattus), prevalences within intermediate snails ranged from 0.2 to 4.8%. Whatever the transmission season may be (rainy vs. dry), most of the infected snails were spatially aggregated and 88.4% of them harbored a single parasite genotype indicative of a monomiracidial infection; 4.7% had dual sex infections and a parasite intensity not exceeding 3 miracidia per snail. A substantial resistance level toward the parasite and recruitment regulatory process within snails may explain in part the observed low parasite prevalences and intensities. Considering such a distribution pattern of larval S. mansoni genetic diversity among B. glabrata, mobility of the definitive hosts, or rapid turnover of infected snails, or both, are required to maintain genetic heterogeneity within adult schistosome populations.

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.

Isolation of microsatellite markers in the digenetic trematode Schistosoma mansoni from Guadeloupe island.

© 2000 Blackwell Science Ltd, Molecular Ecology, 9, 993–1011 De Garcia Leon FJ, Cannone M, Quillet E, Bonhomme F, Chatain B (1998) The application of microsatellite markers to breeding programmes in the sea bass, Dicentrarchus labrax. Aquaculture, 159, 303–316. Hillier L, Green P (1991) OSP: a computer program for choosing PCR and DNA sequencing primers. PCR Methods and Applications, 1, 124–128. O’Reilley P, Wright JM (1995) The evolving technology of DNA fingerprinting and its application to fisheries and aquaculture (1995). Journal of Fish Biology, 47, 29–55. Sambrook J, Fritsh EF, Maniatis T (1989) Molecular Cloning: a Laboratory Manual 2nd edn. Cold Spring Harbor Laboratory Press, New-York. Stepien CA, Faber JE (1998) Population genetic structure, phylogeography and spawning philopatry in walleye (Stizostidion vitreum) from mitochondrial DNA control region sequence. Molecular Ecology, 7, 1757–1769. Todd TN, Hatcher CO (1993) Genetic Variability and Glacial Origins of Yellow perch (Perca flavescens) in North America. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1828–1834. Wirth T, Saint-Laurent R, Bernatchez L (1999) Isolation and characterization of microsatellite loci in the walleye (Stizostedion vitreum), and cross-amplification within the family Percidae. Molecular Ecology, 8, 1961–1963.

Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms.

Coevolutionary dynamics in host-parasite interactions potentially lead to an arms race that results in compatibility polymorphism. The mechanisms underlying compatibility have remained largely unknown in the interactions between the snail Biomphalaria glabrata and Schistosoma mansoni, one of the agents of human schistosomiasis. This review presents a combination of data obtained from field and laboratory studies arguing in favor of a matching phenotype model to explain compatibility polymorphism. Investigations focused on the molecular determinants of compatibility have revealed two repertoires of polymorphic and/or diversified molecules that have been shown to interact: the parasite antigens S. mansoni polymorphic mucins and the B. glabrata fibrinogen-related proteins immune receptors. We hypothesize their interactions define the compatible/incompatible status of a specific snail/schistosome combination. This line of thought suggests concrete approaches amenable to testing in field-oriented studies attempting to control schistosomiasis by disrupting schistosome-snail compatibility.

Sex‐specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications

We studied the population genetic structure of 360 and 1247 adult Schistosoma mansoni using seven microsatellite and seven random amplified polymorphic DNA (RAPD) markers, respectively. Parasites were collected from their natural definitive host Rattus rattus in Guadeloupe (West Indies). We found a sex‐specific genetic structure, a pattern never before reported in a parasitic organism. Male genotypes were more randomly distributed among rats than female genotypes. This interpretation was consistent with a lower differentiation between hosts for males relative to females, the higher genetic similarity between females in the same host and the observed local (i.e. within‐individual‐host) differences in allele frequencies between the two sexes. We discuss our results using ecological and immunological perspectives on host–parasite relationships. These results change our view on the epidemiology of schistosomiasis, a serious disease affecting humans in African and American intertropical zones.

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.