According to the Red Queen hypothesis for sex, cross-fertilization should be positively associated with the probability of exposure (risk) to virulent parasites. Unfortunately, risk is difficult to measure in the wild, and prevalence of infection is often substituted for risk. Here I suggest that prevalence of infection may not generally suffice as a surrogate for risk, since the Red Queen model can make opposite predictions depending on the distribution of risk in the wild. Specifically, the results of a matching-alleles model suggest that asexual populations should be more infected than sexual populations, when (1) the variance in risk among populations is small, and (2) the mean risk of exposure to parasites is near the point where selection switches to favouring sex over asex. If, however, the variance in risk among populations is large, sexual reproduction should be positively associated with the prevalence of infection. In addition, the coefficient of variation for reproductive mode should increase sharply at the switch point. In light of these results, I re-evaluated data from two studies on the distribution of males in 95 populations of a freshwater snail (Potamopyrgus antipodarum). Populations of these snails are often mixtures of sexual and asexual individuals, and the frequency of males is correlated with the frequency of sexual females in the population. The results show a large, highly skewed variance among populations for prevalence of infection by larval trematodes. The results also show a positive, significant relationship between prevalence of infection and the frequency of males, with a sharp increase in the coefficient of variation at intermediate prevalence. In addition, experimental studies suggest that some of the necessary conditions of the Red Queen hypothesis are also met in this system. Specifically, the most common trematode infecting these snails is (1) adapted to infecting local host populations of the snail, and is (2) more infective to clones that were common in the recent past. It is too early to know if the parasite theory is sufficient to explain the widespread distribution of sex. I suggest that the theory is not sufficient, but that parasites in combination with mutation accumulation in clonal lines may explain the maintenance of sex in species that occasionally produce apomictic mutants.

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.

In stark contrast to the huge body of theoretical work on the importance of hosts and parasites as selective agents acting on each other, until recently, little systematic empirical investigation of this issue has been attempted. Research on snail–schistosome interactions have, therefore, the potential for making an important contribution to the study of coevolution or reciprocal adaptation. This may be particularly pertinent since snail–schistosomes represent an indirectly transmitted macroparasite system, so often overlooked amongst both theoretical and empirical studies. Here we review ideas and experiments on snail–schistosome interactions, with particular emphasis on those that may have relevance to the potential coevolution between host resistance and parasite infectivity and virulence. We commence with an introduction and definition of the general concepts, before going into detail of some specific studies to illustrate these: evidence of snail–schistosome coevolutionary process in the field; evidence of coevolutionary processes in the laboratory; a general assessment of the applicability of coevolutionary models in snail–schistosome interactions; and finishing with a section on conclusions and areas for further study.

This paper presents a perspective on the ecology of trematodes in snail hosts based on recent evidence. Because flukes use snails almost obligatorily as first intermediate hosts, we highlight the role of gastropods as keystone species for trematodes and their communities. After reviewing recent developments in the transmission of trematodes to and from snails, we discuss trematode communities within individual snails (infracommunities) and in snail populations (component communities). Results garnered using various protocols at the infracommunity level are reviewed. The few data available, all from marine systems, indicate that low colonization rates characterize infracommunities, suggesting that trematode infracommunities tend to be isolationist in character rather than interactive. The variety of trematode species present in a component community seems to be determined by spatial overlap of definitive hosts. Relative abundance of species in a component community shows little dependence on negative interspecific interactions at the level of the infracommunity. Temporal aspects of trematode communities are related to the life history of the host snail. The component communities of long-lived snails (mostly marine) integrate many infection episodes whereas shorter-lived snails (mostly freshwater) acquire new component communities each time host cohorts turnover.

Irrigation for intensive sugar cultivation started in the early 1980s at Richard Toll, some 100 km from the mouth of the Senegal River. Infections with Schistosoma mansoni were first seen in late 1988. This study records quantitative snail surveys for over 3 years from 1992 at sites representing different habitats in and around the irrigation scheme. Populations of both Biomphalaria pfeifferi (the intermediate host of S. mansoni) and Bulinus spp. (mainly B. truncatus, the local host of S. bovis) peaked in late ‘spring' or early ‘summer', depending on the habitat, and then remained low until the following ‘spring'. B. pfeifferi favoured smaller, man-made habitats with most transmission between May and August each year. The less abundant Bulinus spp. favoured larger natural and man-made habitats with most S. bovis transmission between April and July. S. mansoni infections were more, but S. bovis infections were less abundant than other trematodes in their respective snail hosts. Ecological changes in the early 1980s due to sugar irrigation pre-dated similar, more widespread changes in the late 1980s when the completion of dams across the Senegal River prevented seasonal rain fed floods and sea water intrusion. S. mansoni has since spread rapidly around Richard Toll. The incompatibility of the local S. haematobium strains with the dominant bulinid snails has so far prevented an epidemic of urinary schistosomiasis at Richard Toll, but the invasion of similar downstream habitats by susceptible B. globosus is worrying. The principal control measure, chemotherapy, given in the ‘winter' would minimise the rate of reinfection. It could be reinforced by judicious mollusciciding within the sugar irrigation scheme but not elsewhere.

An epidemiological study on dicrocoeliosis caused by Dicrocoelium dendriticum was carried out on sheep, molluscs and ants in the mountains of León province (NW Spain) between 1987–1991. The results concerning the intermediate hosts and a review of some aspects of dicrocoeliosis are summarized. Mollusc collection for the helminthological study was random throughout the study area at fortnightly intervals. Twenty-nine Gastropoda species were identified. D. dendriticum infection was only detected in 2·98% of the 2084 Helicella itala examined and in 1·06% of 852 H. corderoi. The highest infection prevalence was detected in H. itala in September and in H. corderoi in February. Daughter sporocysts with well-developed cercariae predominated in spring and autumn. Infection prevalence increased with mollusc age and size. Ants were collected from anthills or plants to which they were attached. The behaviour of ants in tetania was followed. Twenty-one Formicidae species were identified, but only the following harboured D. dendriticum: Formica cunicularia (1158 examined specimens, 0·69% infection prevalence, 2–56 metacercariae per ant); F. sanguinea (234, 1·28%, 2–63); F. nigricans (1770, 4·97%, 1–186); F. rufibarbis (288, 6·59%, 2–107). In a flat area close to León town, 95·39% of the 2085 F. rufibarbis specimens collected in tetania contained metacercariae (1–240) in the abdomen. These were used for parasite characterization by isoelectric focusing and to infect lambs and hamsters. Only one brainworm per ant was found.

Fascioliasis due to the digenean species Fasciola hepatica has recently proved to be an important public health problem, with human cases reported in countries of the five continents, including severe symptoms and pathology, with singular epidemiological characteristics, and presenting human endemic areas ranging from hypo- to hyperendemic. One of the singular epidemiological characteristics of human fascioliasis is the link of the hyperendemic areas to very high altitude regions, at least in South America. The Northern Bolivian Altiplano, located at very high altitude (3800–4100 m), presents the highest prevalences and intensities of human fascioliasis known. Sequences of the internal transcribed spacers ITS-1 and ITS-2 of the nuclear ribosomal DNA of Altiplanic Fasciola hepatica and the intermediate snail host Lymnaea truncatula suggest that both were recently introduced from Europe. Studies were undertaken to understand how the liver fluke and its lymnaeid snail host adapted to the extreme environmental conditions of the high altitude and succeeded in giving rise to high infection rates. In experimental infections of Altiplanic lymnaeids carried out with liver fluke isolates from Altiplanic sheep and cattle, the following aspects were studied: miracidium development inside the egg, infectivity of miracidia, prepatent period, shedding period, chronobiology of cercarial emergence, number of cercariae shed by individual snails, survival of molluscs at the beginning of the shedding process, survival of infected snails after the end of the shedding period and longevity of shedding and non-shedding snails. When comparing the development characteristics of European F. hepatica and L. truncatula, a longer cercarial shedding period and a higher cercarial production were observed, both aspects related to a greater survival capacity of the infected lymnaeid snails from the Altiplano. These differences would appear to favour transmission and may be interpreted as strategies associated with adaptation to high altitude conditions.

The results of the studies on our model combination Trichobilharzia ocellata–Lymnaea stagnalis, presented in this review, lead to the conclusion that schistosomes use multiple strategies to reach their goals, i.e. to propagate and to continue their life cycle. They have to escape from being attacked by the internal defence system (IDS) of the snail host and to profoundly affect the host's energy flow, of which reproduction and growth are the main determinants, for their own benefit. These physiological changes they establish mainly by interfering with the two regulatory systems in the snail host, the IDS and the neuroendocrine system (NES). Moreover, these two regulatory systems clearly interact with each other. Parasitic E/S products affect the host's IDS both in a direct and an indirect way. The neuropeptides or neuropeptide-like substances that are secreted by parasite glands into the host directly suppress haemocyte activity in the snail. The indirect effects include effects of (1) peptides from connective tissue cells and (2) neuropeptides from NES and/or IDS. Parasitic E/S products also induce the effects on energy flow in the host. These E/S products act either directly on a target, as shown for the inhibiting effect of the parasite on the development of the male copulation organ, or on the NES regulating reproductive activity, e.g. on gene expression. Indirect effects of E/S products on the NES (hormone-receptor interaction, electrical activity) are mediated by a factor from connective tissue cells, presumably belonging to the IDS. The physiological changes in the snail host are obviously of vital importance for the parasites, since they make use of different strategies to bring them about.

Although the effects of trematode infection on snail host physiology or host responses on parasite development have been well described in the literature, very little is known regarding the underlying mechanisms and specific molecules responsible for mediating those effects. It is presumed that many host–parasite interactions are communicated through receptor-mediated events, in particular those involving haemocytic immune responses to invading parasites, larval motility and migration through host tissues, and larval acquisition of host molecules either as nutrients or critical developmental factors. The intent of this chapter is to review current knowledge of molecules (both receptors and their ligands or counter-receptors) involved in molecular communication at the interface between larval trematodes, especially the mother or primary sporocyst stage, and host cells/tissues in intimate proximity to developing larvae. Information to date suggests that the molecular exchange at this interface is a highly complex and dynamic process, and appears to be regulated in specific cases. Topics discussed will focus on snail cell receptor interactions with the sporocyst tegument and its secretions, host cell–cell and cell–substrate adhesion receptors and their related signal transduction pathways, and sporocyst tegumental surface receptors and ligands involved in the binding of soluble host molecules.

In parallel with massive research efforts in human schistosomiasis over the past 30 years, persistent efforts have been made to understand the basis for compatibility and incompatibility in molluscan schistosomiasis. Snail plasma contains molecules that are toxic to trematodes, but these seem to kill only species that never parasitize the mollusc used as the source of plasma. A sporocyst will be killed actively by haemocytes alone if they are from a snail that is resistant to the trematode. Oxygen-dependent killing mechanisms play a major role. Enzymes such as NADPH oxidase, superoxide dismutase, myeloperoxidase and nitric oxide synthase are critical components of the putative killing pathways. Metabolic intermediates such as hydrogen peroxide and nitric oxide appear to be more important against trematodes than the shorter-lived intermediates that are more important in anti-microbial defences. Products secreted by trematode larvae influence the physiology of snail haemocytes, implying active counter-defences mounted by the parasite, but these remain largely unexplored. A possible molecular basis for the susceptibility/resistance dichotomy in molluscan schistosomiasis is suggested to be deficient forms of enzymes in the respiratory burst pathway, and a selective disadvantage for schistosome resistance is an integral component of this model.

Biomphalaria glabrata is a major intermediate host for the helminth parasite Schistosoma mansoni. Beginning in the mid-20th century, studies were carried out with this snail species to identify the immunological and genetic components that might be involved in controlling schistosome development. A number of genetically well-defined snail stocks were derived as a direct result of these studies and have since played major roles in helping investigators to identify important cellular and humoral components in the snail/schistosome relationship. This review will explore the historical development of these stocks and describe some of the major advances in several areas of medical malacology that have been made possible by their use.

Gene mapping and the generation of linkage groups are fundamental to an understanding of the organization and relationships of genes and marker sequences, providing a framework with which to investigate their association with traits of interest. The abundance of techniques available for generating polymorphic molecular markers, and recent advances in high throughput screening, have allowed the extension of map analysis to the tropical freshwater snail Biomphalaria glabrata, an important intermediate host for Schistosoma mansoni. Direct comparison of gene expression by differential display screening, without prior identification of candidate genes, can be combined with mapping to quantify the involvement of specific sequences in the schistosome resistance response, and other important host–parasite interactions. Here we discuss the application of current and emergent technologies to gene characterization and linkage analysis in snail–schistosome interactions. Preliminary results from the analysis of comparative gene expression in resistant and susceptible snails are also presented.

Freshwater snails belonging to the genus Biomphalaria are intermediate hosts of the trematode Schistosoma mansoni in the Neotropical region and Africa. In Brazil, one subspecies and ten species of Biomphalaria have been identified: B. glabrata, B. tenagophila, B. straminea, B. occidentalis, B. peregrina, B. kuhniana, B. schrammi, B. amazonica, B. oligoza, B. intermedia and B.t. guaibensis. However, only the first three species are found naturally infected with S. mansoni. The classical identification of these planorbids is based on comparison of morphological characteristics of the shell and male and female reproductive organs, which is greatly complicated by the extensive intra-specific variation. Several molecular techniques have been used in studies on the identification, genetic structure as well as phylogenetic relationships between these groups of organisms. Using the randomly amplified polymorphic DNAs (RAPD) analysis we demonstrated that B. glabrata exhibits a remarkable degree of intra-specific polymorphism. Thus, the genetics of the snail host may be more important to the epidemiology of schistosomiasis than those of the parasite itself. Using the simple sequence repeat anchored polymerase chain reaction (SSR-PCR) in intra-populational and intra-specific studies we have demonstrated that snails belonging to the B. straminea complex (B. straminea, B. kuhniana and B. intermedia) clearly presented higher heterogeneity. Using the low stringency polymerase chain reaction (LS-PCR) technique we were able to separate B. glabrata from B. tenagophila and B. tenagophila from B. occidentalis. To separate all Brazilian Biomphalaria species we used the restriction fragment length polymorphism (PCR-RFLP) of the internal transcribed spacer region (ITS) of the DNA gene. The method also proved to be efficient for the specific identification of DNA extracted from snail eggs. Recently we have sequenced the ITS2 region for phylogenetic studies of all Biomphalaria snails from Brazil.

Schistosoma mansoni is one of the most abundant infectious agents of humankind. Its widespread distribution is permitted by the broad geographic range of susceptible species of the freshwater snail genus Biomphalaria that serve as obligatory hosts for its larval stages. Molecular phylogenetic studies suggest that Schistosoma originated in Asia, and that a pulmonate-transmitted progenitor colonized Africa and gave rise to both terminal-spined and lateral-spined egg species groups, the latter containing S. mansoni. Schistosoma mansoni likely appeared only after the trans-Atlantic dispersal of Biomphalaria from the Neotropics to Africa, an event that, based on the present African fossil record, occurred only 2–5 million years ago. This parasite became abundant in tropical Africa and then entered the New World with the slave trade. It prospered in the Neotropics because a remarkably susceptible and productive host, B. glabrata, was widely distributed there. Indeed, a snail similar to B. glabrata may have given rise to the African species of Biomphalaria. Schistosoma mansoni has since spread into other Neotropical Biomphalaria species and mammalian hosts. The distribution of S. mansoni is in a state of flux. In Egypt, S. mansoni has nearly completely replaced S. haematobium in the Nile Delta, and has spread to other regions of the country. A susceptible host snail, B. straminea, has been introduced into Asia and there is evidence of S. mansoni transmission in Nepal. Dam and barrage construction has lead to an epidemic of S. mansoni in Senegal, and the parasite continues its spread in Brazil. Because of competition with introduced aquatic species and environmental changes, B. glabrata and consequently S. mansoni have become less abundant on the Caribbean islands. Control of S. mansoni using praziquantel and oxamniquine has reduced global prevalence but control is difficult to sustain, and S. mansoni can develop tolerance/resistance to praziquantel, raising concerns about its future efficacy. Because of legitimate environmental concerns, snail control is unlikely to be an option in future control efforts. Global warming will impact the distribution of Biomphalaria and S. mansoni, but the magnitude and nature of the effects are poorly understood.

Snails and digeneans have been associated for at least 200 million years. Their inter-relationships over such a time-span must have been complex and varied. Few studies have attempted to explore these relationships in the light of knowledge of the phylogeny of both host and parasite groups. Here we focus on two important families of digeneans, the Schistosomatidae and the Paragonimidae, for which molecular phylogenies are available. We investigate the types of evolutionary relationships between host and parasite, operating at different phylogenetic depths, that might explain current host specificity and distributions of both associates. Both families of parasites utilise a number of highly diverged gastropod families, indicating that host extensions have featured in their histories. However, schistosomatids and paragonimids show different patterns of association with their snail hosts. As befits the apparently more ancient group, schistosomatids utilise snails from across a wide phylogenetic range within the Gastropoda. The genus Schistosoma itself has experienced one long-range host switch between pulmonates and caenogastropods. By contrast, paragonimids are restricted to two superfamilies of caenogastropods. Despite these differences, modern schistosomatid species appear to be more host specific than are paragonimids and host additions, at the level of host family, are far less common among species of schistosomatids than among paragonimids. Some species of Paragonimus exhibit remarkably low levels of host specificity, with different populations utilising snails of different families. Existing knowledge relating to the phenomenon will be presented in the context of phylogenies of schistosomatids, paragonimids, and their snail hosts. Discussion focuses on the usefulness of current theories of snail–digenean coevolution for interpreting these findings. In the past, much emphasis has been placed on the idea that digeneans engage in a one-to-one arms race with their snail host. We consider that phylogenetic tracking rather than an arms-race relationship might be a common alternative. Not being bound by the restrictions imposed by an arms race, some digeneans might be able to extend to new host species more easily than the literature suggests. Switches into related host taxa are most likely. However, ecologically equivalent but unrelated gastropod hosts may also be exploited. Given the right ecological setting, digeneans are able to switch across considerable phylogenetic distances. Examples from the Paragonimidae and Schistosomatidae are given.

Within each of the four species groups of Bulinus there are species that act as intermediate hosts for one or more of the seven species of schistosomes in the Schistosoma haematobium group, which includes the important human pathogens S. haematobium and S. intercalatum. Bulinus species have an extensive distribution throughout much of Africa and some surrounding islands including Madagascar, parts of the Middle East and the Mediterranean region. Considerable variation in intermediate host specificity can be found and differences in compatibility between snail and parasite can be observed over small geographical areas. Molecular studies for detection of genetic variation and the discrimination of Bulinus species are reviewed and two novel assays, allele-specific amplification (ASA) and SNaPshot™, are introduced and shown to be of value for detecting nucleotide changes in characterized genes such as cytochrome oxidase 1. The value and complexity of compatibility studies is illustrated by case studies of S. haematobium transmission. In Senegal, where B. globosus, B. umbilicatus, B. truncatus and B. senegalensis may act as intermediate hosts, distinct differences have been observed in the infectivity of different isolates of S. haematobium. In Zanzibar, molecular characterization studies to discriminate between B. globosus and B. nasutus have been essential to elucidate the roles of snails in transmission. B. globosus is an intermediate host on Unguja and Pemba. Further studies are required to establish the intermediate hosts in the coastal areas of East Africa. Biological factors central to the transmission of schistosomes, including cercarial emergence rhythms and interactions with other parasites and abiotic factors including temperature, rainfall, water velocity, desiccation and salinity are shown to impact on the intermediate host-parasite relationship.

Of the four species of Bulinus found on Madagascar, three species: B. obtusispira, B. liratus and B. bavayi are endemic while the fourth, B. forskalii, is probably a recent introduction from the African mainland. The evolutionary relationships of these species with Bulinus species from Africa were studied by phylogenetic analysis of DNA sequence variation at two mitochondrial loci: cytochrome oxidase subunit I (COI) and large ribosomal subunit (LSU) or 16S. The observed levels of nucleotide divergence within Bulinus were substantial but may underestimate the true levels as there was evidence of ‘saturation' of transitional substitutions at both loci. A putative secondary structure model for the sequenced segment of the 16S was developed. Subsequent phylogenetic analysis using transversional changes only for both loci, showed that there were contrasting levels of divergence within the four species groups. B. obtusispira was consistently placed within the B. africanus group, appearing ancestral to this group and was closest to the basal node within Bulinus. Together with B. bavayi, the two species appear to have been isolated on Madagascar for a long time, contrasting with both B. liratus and B. forskalii that appear more recent colonisers; however, estimate of exact times of divergence is problematic. A PCR-RFLP assay was developed to enable identification and discrimination of B. obtusispira and B. liratus using discriminatory variation within the COI. To enable population genetic analysis within B. obtusispira, microsatellite markers were developed using an enrichment method and 8 primer pairs are reported. Laboratory infection experiments using Madasgacan S. haematobium from the Mahabo area showed that certain populations of B. obtusispira, B. liratus and B. bavayi were compatible.

Freshwater snails of the Bulinus forskalii group are one of four Bulinus species complexes responsible for the transmission of schistosomes in Africa and adjacent regions. The species status of these conchologically variable and widely distributed planorbids remains unclear, and parasite compatibility varies considerably amongst the eleven taxa defined, making unambiguous identification and differentiation important prerequisites for determining their distributions and evolutionary relationships. Random Amplified Polymorphic DNA (RAPD) analyses were used to investigate relationships between taxa, with particular emphasis on Central and West African representatives. RAPD-derived phylogenies were compared with those from other independent molecular markers, including partial sequences of mitochondrial cytochrome oxidase subunit I (COI) gene, and the nuclear ribosomal RNA internal transcribed spacer 1 region (ITS1). The phylogenetic reconstructions from the three approaches were essentially congruent, in that all methods of analysis gave unstable tree topologies or largely unresolved branches. There were large sequence divergence estimates between species, with few characters useful for determining relationships between species and limited within species differentiation. Nuclear and mtDNA sequence data from Central and East African representatives of the pan-African B. forskalii showed little evidence of geographical structuring. Despite the unresolved structure within the phylogenies, specimens from the same species clustered together indicating that all methods were capable of differentiating taxa but could not establish the inter-specific relationships with confidence. The limited genetic variation displayed by B. forskalii, and the evolution and speciose nature of the group, are discussed in the context of the increasingly arid climate of the late Miocene and early Pliocene of Africa.

Life history traits expressed by organisms vary due to ecological and evolutionary constraints imposed by their current environmental conditions and genetic heritage. Trematodes often alter the life history of their host snails by inducing parasitic castration. Our understanding of the variables that influence the resulting changes in host growth, fecundity and survivorship is insufficient to confidently predict specific outcomes of novel snail–trematode combinations. In a literature review of the last 30 years, we found 41 publications examining various life history characteristics of trematode-infected snails. These publications reported 113 different field and laboratory experiments involving 30 snail species and 39 trematode species and provided a data set for assessing factors that potentially affect life history outcomes. Analysis of the diverse responses across various snail–trematode systems and experimental conditions teased out general patterns for the expression of host growth, fecundity and survival. These were used to address existing hypotheses and develop several new ones relating the response of snail-trematode interactions to environmental and genetic factors. Finally, we propose directions for future experiments that will better assess the ecological and evolutionary factors influencing snail life history responses to trematode parasitism.