SELECTION AND STRAIN SPECIFICITY OF COMPATIBILITY BETWEEN SNAIL INTERMEDIATE HOSTS AND THEIR PARASITIC SCHISTOSOMES

Many theoretical models of host-parasite coevolution assume that variation in host resistance to parasite infection is, at least partially, genetically determined and specific to the strain of infecting parasite. However, very few experimental studies have been conducted to test this assumption in animal-parasite systems. Biomphalaria glabrata snails serve as the intermediate hosts of Schistosoma mansoni. Although some snails are resistant to infection, there is no evidence of fixation of resistance in field populations. Two possible explanations for this are high fitness costs associated with resistance and a dynamic coevolution between parasite and host, perhaps involving matching alleles or gene-for-gene interactions. Two strains of B. glabrata were artificially selected for either resistance or susceptibility to each of two strains of S. mansoni parasite for three generations. Third-generation snails were then were exposed to either the parasite strain to which they had been selected or to a different parasite strain. In both host strains, resistance and susceptibility (compatibility) were found to be heritable. Moreover, compatibility to one parasite strain was not associated with compatibility to another strain, implying no genetic trade-off. Our results are discussed in terms of potential mechanisms of resistance in this host-parasite system and their implications to general coevolutionary theory.     

Parasite infection,host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite

Parasites have been proposed to be fundamental in the evolution of mate choice because differential mating on the basis of heritable disease resistance is expected to lead to progeny with a better genome-environment match than random mating. However, direct empirical data in support of this hypothesis are often lacking, and the relative influences of current and potential infection status (i.e. resistance genotype), and of mate choice versus mate conflict, remain largely unknown. We demonstrate experimentally, using simultaneous hermaphroditic snails (Biomphalaria glabrata) artificially selected for resistance or susceptibility to Schistosoma mansoni infection, that mate choice is influenced by a combination of current and potential parasitic infection status. As predicted by game-theory models, we also found a picture of conflict and cooperation: resistant and susceptible genotypes copulated in either gender and reciprocated (i.e. switched gender) equally when faced with an uninfected partner, but, by contrast, resistant snails actively refused to copulate as females with an infected partner. Such recognition and discrimination has implications for the maintenance of sex and the evolution of recognition systems.     

Mate choice, frequency dependence, and the maintenance of resistance to parasitism in a simultaneous hermaphrodite

Biomphalaria glabrata are simultaneous hermaphroditic freshwatersnails that act as intermediate hosts for the macroparasitictrematode Schistosoma mansoni, a causative agent of schistosomiasis.Heritability and strain-specificity of both snail resistanceand susceptibility to schistosome infection have been demonstrated,genetic variability for which is maintained, in part, throughtrade-offs between high fitness costs associated with infectionand those associated with resistance. However, despite sucha high cost of resistance and a low prevalence of infectionin natural snail populations, genes for resistance are maintainedwithin snail populations over successive generations, includingin the complete absence of parasite pressure in laboratory populations.This may be indicative of alternative benefits of resistancegenes, in addition to parasite defense, such as differentialmating success between genotypes. Here we examined the mateand gender choice of snails across a multi-factorial range ofpotential partner combinations. These included host-resistanceor susceptibility genotype, host genotype frequency within thepopulation, current parasite infection status, and parasitegenotype. We demonstrate recognition and discrimination by hostsnails depending on host and/or parasite genotype for each ofthese factors. In particular, our results suggest that a raremating advantage to resistant genotypes may be a potential explanationfor the maintenance of highly costly resistance genes withinintermediate host populations under conditions of low or zeroparasite pressure.     

Host reproductive fitness: the influence of increasing parasite pressure in a Biomphalaria glabrata/Schistosoma mansoni system

Summary

Host life history traits are often shaped by trade-offs between the current and potential future costs of parasitism. Reproductive tissues are not normally essential for host survival and diversion of resources elsewhere is a common effect of parasitic infection. Variations in reproductive output may therefore indicate overall fitness correlated to the host response to parasite pressure. Here, we investigated reproductive fitness in a Biomphalaria glabrata—Schistosoma mansoni system, a laboratory model for schistosomiasis. Five matched groups of unselected B. glabrata snails were individually exposed to doses of 1, 2, 5, 10 or 20 S. mansoni miracidia, respectively. A sixth group remained unexposed providing a control. Fertility (defined as actual reproductive performance, measured as the number of offspring produced) and fecundity (defined as potential reproductive capacity, measured as number of eggs and embryos formed) were monitored for each group at weekly intervals. Our results revealed that both parasite dose and infection status had a significant effect on the potential reproductive capacity of the host, but this was not always reflected in the actual reproductive success. Egg mass production showed a negative association with increasing parasite dose in patently infected snails. In contrast, snails exposed to the parasite, but within which infection did not establish, demonstrated a positive association between egg mass production and parasite dose. This suggests the existence of a fecundity compensation mechanism occurring within the post-patent period of infection. This is, to our knowledge, the first report of such an effect in a snail-trematode system and, indeed, in any host-parasite association.     

Hemocytes from neonates of Biomphalaria glabrata are functionally less mature than those from adult snails

Gastropod molluscs, which serve as obligatory intermediate hosts for digenetic trematodes, possess an internal defense system (IDS) consisting of phagocytic hemocytes and plasma factors. This IDS is responsible for resistance to infection with larval trematodes, which are encapsulated and killed by hemocytes in incompatible snails. Like other physiological systems, the IDS probably undergoes maturation during early stages of life, and the relatively undeveloped state of the IDS in young snails has been hypothesized to be a factor in their increased susceptibility to infection with larval trematodes. In this study, hemocytes were examined in the BS-90 laboratory strain of Biomphalaria glabrata that is resistant to infection with Schistosoma mansoni as adults but susceptible to infection as neonates. Compared with hemocytes from adults, hemocytes from neonates had a smaller perimeter and lower intrinsic directional motility on glass microscope slides. Additionally, in vitro assays showed a lower association with fucoidan-linked polystyrene beads and less ability to produce superoxide anion in hemocytes from neonates compared to hemocytes from adults. These results support the hypothesis that the gastropod IDS undergoes maturation during growth. However, whether the observed differences between hemocytes of neonatal and adult BS-90 snails play a role in the susceptibility of the former and resistance of the latter to infection with S. mansoni is not known.     

Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system

Natural host populations often exhibit genetic variability in resistance to parasitism. One possible mechanism for maintaining such diversity is a trade-off between fitness costs associated with resistance and fitness costs associated with parasitism. However, little is known about the nature or magnitude of these costs in animal populations. Using artificial selection experiments in a Biomphalaria glabrata–Schistosoma mansoni host–parasite system, we demonstrated that resistance and susceptibility to infection are heritable. We then investigated whether resistance had any associated costs in terms of snail reproductive success. Susceptible-selected snail lines showed significantly higher fertility (number of offspring produced) than resistant-selected or unselected control snail lines, irrespective of current infection status. There were no consistent differences between snail lines in fecundity, proportion of abnormal egg masses produced, or mean number of eggs per egg mass. Mortality rate was higher among infected than uninfected snails. These results are consistent with snails incurring costs of resistance to schistosome infection in the absence of the parasite.     

Phylogenetic relationships between Lymnaeidae in relation to infection with Fasciola sp. in Hokkaido,Japan

ABSTRACT

In this paper, lymnaeid snails collected from 107 localities in Hokkaido, Japan were examined for infection by Fasciola larvae. DNA sequences from the snails were analysed phylogenetically based on their mitochondrial cytochrome c oxidase (COI) gene. Based on shell morphology, the snails were identified as Galba truncatula, Radix auricularia, and Austropeplea ollula and were divided into distinct clades in the COI tree. No Fasciola larvae were detected in any of the collected snails. The 58 haplotypes of Galba truncatula which were found in Hokkaido included five detected previously in snails infected with Fasciola larvae, and constituted a closely related haplogroup (Gt-c1), suggesting that Gt-c1 snails would be susceptible to Fasciola sp. The Gt14 haplotype snails were considered to be Lymnaea schirazensis, an intermediate host of F. hepatica. The COI haplotypes of A. ollula belonged to a single clade, and were considered conspecific, whereas those of R. auricularia constituted three genetically distinct haplogroups, each of which was possibly a distinct species. This study suggests that morphologically-identified lymnaeid snails possibly include additional species. Further study of these snails is required to clarify their susceptibility to Fasciola sp.     

Diet alters delayed selfing,inbreeding depression,and reproductive senescence in a freshwater snail

Reproductive success is a critical fitness attribute that is directly influenced by resource availability. Here, we investigate the effects of diet‐based resource availability on three interrelated aspects of reproductive success: a change in mating system based on mate availability, consequent inbreeding depression, and the deterioration of reproductive efficiency with age (senescence). We employed a factorial experimental design using 22 full‐sib families of the hermaphroditic freshwater snail Physa acuta to explore these interactions. Individual snails were reared in one of two mate‐availability treatments (isolated [selfing] or occasionally paired [outcrossing]) and one of two diet treatments (boiled lettuce or Spirulina, an algae that is rich in protein, vitamins, and minerals). Spirulina‐fed snails initiated reproduction at a 13% earlier age and 7% larger size than lettuce‐fed snails. Spirulina also resulted in a 30% reduction in the time delay before selfing. Compared to lettuce, a diet of Spirulina increased inbreeding depression by 52% for egg hatching rate and 64% for posthatching juvenile survival. Furthermore, Spirulina led to a 15‐fold increase in the rate of reproductive senescence compared with a diet of lettuce. These transgenerational, interactive effects of diet on inbreeding depression and reproductive senescence are discussed in the context of diet‐induced phenotypic plasticity.     

Genotypic variation in induced resistance and induced susceptibility in the peach-Myzus persicae aphid system

In response to herbivore damage or stress, plants may express physiological or morphological changes known as induced responses. We tested whether previous herbivory by the aphid Myzus persicae differentially altered the expression of resistance and susceptibility among five genotypes of peach that differ in their resistance phenotype (avoidance resistance, antibiosis resistance or susceptibility). We measured behavioural and performance parameters of aphid success on plants previously infested by conspecifics as compared to uninfested controls. Significant variation was found both among genotypes and among resistance phenotype, including between genotypes showing a same resistance phenotype. Genotypes with avoidance resistance showed either induced resistance to aphid settling or no response. Genotypes with antibiosis resistance showed induced susceptibility to aphid settling, but the effects of previous herbivory on aphid development were either positive or negative depending on the genotype. In the susceptible genotype, most parameters of aphid settlement and performance, including reproduction, were positively influenced by previous herbivory. Using electronic recording, the aphid probing behaviour was examined to tentatively identify host plant tissues most likely to play a role in induced defenses. Probing behaviour was significantly affected by plant genotype, previous herbivory, and their interaction, indicating complex relations between the two factors. In the genotypes with avoidance resistance, aphids were deterred before they reach the phloem. In the genotypes expressing susceptibility or antibiosis resistance, previous herbivory triggered instead the induction of a phloem‐mediated response, that however diverged depending on the resistance status (facilitation or reduction of phloem sap uptake respectively). Genotypic variation in induction found in the peach‐M. persicae system establishes a useful framework to improve our knowledge of the ecological role of induced plant responses to aphids.     

Identification of a genetic marker associated with the resistance to Schistosoma mansoni infection using random amplified polymorphic DNA analysis

In schistosomiasis, the host/parasite interaction remains not completely understood. Many questions related to the susceptibility of snails to infection by respective trematode still remain unanswered. The control of schistosomiasis requires a good understanding of the host/parasite association. In this work, the susceptibility/resistance to Schistosoma mansoni infection within Biomphalaria alexandrina snails were studied starting one month post infection and continuing thereafter weekly up to 10 weeks after miracidia exposure. Genetic variations between susceptible and resistant strains to Schistosoma infection within B. alexandrina snails using random amplified polymorphic DNA analysis technique were also carried out. The results showed that 39.8% of the examined field snails were resistant, while 60.2% of these snails showed high infection rates.In the resistant genotype snails, OPA-02 primer produced a major low molecular weight marker 430 bp. Among the two snail strains there were interpopulational variations, while the individual specimens from the same snail strain, either susceptible or resistant, record semi-identical genetic bands. Also, the resistant character was ascendant in contrast to a decline in the susceptibility of snails from one generation to the next.     

Males prefer virgin females,even if parasitized,in the terrestrial isopod Armadillidium vulgare

In many species, males increase their reproductive success by choosing high‐quality females. In natural populations, they interact with both virgin and mated females, which can store sperm in their spermatheca. Therefore, males elaborate strategies to avoid sperm competition. In the terrestrial isopod Armadillidium vulgare, females can store sperm and produce several clutches. Moreover, this species can be parasitized by Wolbachia, which feminizes genetic males, transforming them into functional females. Our study compared attractiveness and mate choice when a male is exposed to both virgin and experienced females (i.e., females who have produced offspring and rested for 6 months), with or without Wolbachia. Our results revealed that males are more attracted to virgin females than experienced females, even if these virgin females are parasitized. Moreover, the chemical analysis highlighted different odors in females according to their reproductive and infection (Wolbachia‐free or vertically Wolbachia‐infected) status. Males attempted copulation more frequently and for longer with virgin females, even if Wolbachia‐infected, while experienced females refused further copulation. The evolutionary consequences of both male choice and female resistance on their fitness are discussed in this study.     

The Effects of Isolation,Grouping and Population Density on Fecundity of Bulinus truncatus

Summary

Bulinus truncatus is the intermediate host of Schistosoma haematobium, a trematode parasite causing bladder bilharziasis in man. In the struggle against this disease, control of snail populations is an important goal and expansion of our knowledge of the reproductive activity of Bulinus is relevant in this regard.

In this study the effects of various factors on the fecundity of Bulinus were investigated in specimens kept under continuous water refreshment conditions. The results are considered to be more indicative of the natural situation than results obtained under the current use of discontinuous water refreshment.

Isolated snails produce considerably higher numbers of egg masses and eggs than grouped snails. The effect of grouping on isolated snails, and the reverse situation, is very rapid, being fully effective within one week. The increase in fecundity of isolated snails is most probably caused by the absence of copulatory activity, since transfer of semen is known to curtail egg laying in freshwater pulmonate snails. Egg mass production was shown to decrease with increasing population density. This may be caused either by the difference in space available or by the possible difference in copulatory activity. Isolated snails showed a faster body growth than grouped snails.

The possible role of hormones involved in establishing the above effects and the consequences of the results for snail control programs are discussed.     

Etude experimentale de l' effet du groupement sur la ponte d' Helix aspersa Müller / Experimental study of the effect of population density on egg-laying by the snail Helix aspersa Müller

Summary

The reproductive cycle of Helix aspersa raised under our experimental conditions starts six months after birth.

The experimental grouping of snails influences three aspects of their reproductive activity

1. The rate of egg-laying has been calculated not only in relation to the total number of animals (N1), but also to the number of individuals weighing 8 g or more (N2), and the number of ‘full-grown’ snails.

2. The sexual precocity of the snails is inversely related to the density of the population.

3. The period of reproduction is longer when the density of the population is low.

As with growth, a high density of population has unfavourable mass-effect consequences as regards the proportion of laying snails and the number of layings per animal.     

Mate choice for genetic compatibility in the house mouse

In house mice, genetic compatibility is influenced by the t haplotype, a driving selfish genetic element with a recessive lethal allele, imposing fundamental costs on mate choice decisions. Here, we evaluate the cost of genetic incompatibility and its implication for mate choice in a wild house mice population. In laboratory reared mice, we detected no fertility (number of embryos) or fecundity (ability to conceive) costs of the t, and yet we found a high cost of genetic incompatibility: heterozygote crosses produced 40% smaller birth litter sizes because of prenatal mortality. Surprisingly, transmission of t in crosses using +/t males was influenced by female genotype, consistent with postcopulatory female choice for + sperm in +/t females. Analysis of paternity patterns in a wild population of house mice showed that +/t females were more likely than +/+ females to have offspring sired by +/+ males, and unlike +/+ females, paternity of their offspring was not influenced by +/t male frequency, further supporting mate choice for genetic compatibility. As the major histocompatibility complex (MHC) is physically linked to the t, we investigated whether females could potentially use variation at the MHC to identify male genotype at the sperm or individual level. A unique MHC haplotype is linked to the t haplotype. This MHC haplotype could allow the recognition of t and enable pre‐ and postcopulatory mate choice for genetic compatibility. Alternatively, the MHC itself could be the target of mate choice for genetic compatibility. We predict that mate choice for genetic compatibility will be difficult to find in many systems, as only weak fertilization biases were found despite an exceptionally high cost of genetic incompatibility.     

Dart shooting influences paternal reproductive success in the snail Helix aspersa (Pulmonata, Stylommatophora)

Although animal courtship behaviors are generally understoodwithin the context of sexual selection, the relevance of manysexual behaviors to sexual selection, and vice versa, remainsunexplained. For example, the adaptive function of the "lovedart" used in the precopulatory behavior of hermaphroditicland snails is only now becoming apparent. Contrary to previous assumptions, dart shooting is unlikely to function as a stimulusfor copulation. In searching for a more ultimate explanationof the dart's function, we tested whether variation in dartshooting influences reproductive fitness in Helix aspersa.Individual mother snails were mated sequentially to two potentialfathers. Dart shooting was closely observed and quantifiedfor all pairings, and percentages of offspring sired by each potential father were determined using allozymes. The resultsindicate that snails that shoot darts effectively have significantlygreater paternal reproductive success than snails that shootpoorly. In contrast, there was no significant effect of matingorder on either dart shooting or paternal reproductive success.     

Parasite-induced parthenogenesis in a freshwater snail: stable,persistent patterns of parasitism

Summary The role of parasites in the evolution of host reproductive modes has gained renewed interest in evolutionary ecology. It was previously argued that obligate parthenogenesis (all-female reproduction) arose in a freshwater snail, Campeloma decisum, as a consequence of severe sperm limitation caused by an unencysted trematode, Leucochloridiomorpha constantiae. In the present study, certain conditions are examined for parasitic castration to account for the maintenance of parthenogenesis: the spatial patterns of the prevalence and intensity of infection on a broad geographical scale and its relationship to host genotype; the recovery from infection after isolation from sources of infection; age-related patterns of infections; and the effects of L. constantiae on snail fecundity.In contrast to the common pattern of the aggregated distribution of parasites within host populations, many snail populations with high prevalence and intensity of infection have non-aggregated parasite distributions. Clonal genotype of the host explained little of the variation in intensity and prevalence of infection by the parasite. Female snails maintained similar prevalence and intensity of infection after isolation, and individuals accumulated parasites throughout their lifespan, both of which suggest there is no effective immune response to infection by L. constantiae. Snail fecundity is not significantly influenced by the intensity of infection. These results suggest that L. constantiae may have represented a strong selective force against males during the initial introduction of this parasite into sexual snail populations because of the persistent nature of infection.     

Plant genotype and induced responses affect resistance to herbivores on evening primrose (Oenothera biennis)

Abstract. 1. Although both genotype and induced responses affect a plant's resistance to herbivores, little is known about their relative and interactive effects. This study examined how plant genotype of a native plant (Oenothera biennis) and induced plant responses to herbivory affect resistance to, and interactions among, several herbivores. 2. In a field experiment, genetic and environmental variation among habitats led to variation in the amount of early season damage and plant quality. The pattern of variation in early season infestation by spittlebugs (Philaenus spumarius, a piercing–sucking herbivore) negatively correlated with oviposition preference by a later feeding specialist weevil (Tyloderma foveolatum, a leaf‐chewer). 3. To determine if plant genotype and induced responses to herbivory might be responsible for these field patterns, we performed no‐choice and choice bioassays using four genotypes of O. biennis that varied in resistance. Plants were induced by either spittlebugs or weevils and assays measured the responses of the same specialist weevil as well as a generalist caterpillar (Spodoptera exigua). 4. Resistance to adult weevils was largely unaffected by plant genotype, while they experienced induced resistance following damage by conspecific weevils in no‐choice assays. Caterpillars were more strongly affected by plant genotype than induced responses in both no‐choice and choice assays, but they also fed less and experienced higher mortality on plants previously damaged by weevils. In contrast to the pattern suggested by the field experiment, spittlebugs did consistently induce resistance against either weevils or caterpillars in the bioassay experiment. 5. These results support recent findings that show herbivore species can compete via induced plant responses. Additionally, a quantitative review of the literature demonstrates that plant genotype tends to be more important than interspecific competition among herbivores (plant‐mediated or otherwise) in affecting herbivore preference and performance.