Hybrid fitness in a locally adapted parasite

The parasite (Red Queen) hypothesis for the maintenance of sexual reproduction and genetic diversity assumes that host-parasite interactions result from tight genetic specificity. Hence, hybridization between divergent parasite populations would be expected to disrupt adaptive gene combinations, leading to reduced infectivity on exposure to parental sympatric hosts, as long as gene effects are nonadditive. In contrast, hybridization would not cause reduced infectivity on allopatric hosts unless the divergent parasite populations possess alleles that are intrinsically incompatible when they are combined. In three different experiments, we compared the infectivity of locally adapted parasite (trematode) populations with that of F(1) hybrid parasites when exposed to host (snail) populations that were sympatric to one of the two parasite populations. We tested for intrinsic genetic incompatibilities in two experiments by including one host population that was allopatric to both parasite populations. As predicted, when the target host populations were sympatric to the parasite populations, the hybrids were significantly less infective than the parental average, while hybrid parasites on allopatric hosts were not, thereby ruling out intrinsic genetic incompatibilities. The results are consistent with nonadditive gene effects and tightly specific host-driven selection underlying parasite divergence, as envisioned by coevolutionary theory and the Red Queen hypothesis.     

Contact-based transmission models in terrestrial gastropod populations infected with parasitic mites

Parasite transmission fundamentally affects the epidemiology of host-parasite systems, and is considered to be a key element in the epidemiological modelling of infectious diseases. Recent research has stressed the importance of detailed disease-specific variables involved in the transmission process. Riccardoella limacum is a hematophagous mite living in the mantle cavity of terrestrial gastropods. In this study, we experimentally examined whether the transmission success of R. limacum is affected by the contact frequency, parasite load and/or behaviour of the land snail Arianta arbustorum, a common host of R. limacum. In the experiment the transmission success was mainly affected by physical contacts among snails and slightly influenced by parasite intensity of the infected snail. Using these results we developed two different transmission models based on contact frequencies and transmission probability among host snails. As parameters for the models we used life-history data from three natural A. arbustorum populations with different population densities. Data on contact frequencies of video-recorded snail groups were used to fit the density response of the contact function, assuming either a linear relationship (model 1) or a second-degree polynomial relationship based on the ideal gas model of animal encounter (model 2). We calculated transmission coefficients (β), basic reproductive ratios (R₀) and host threshold population densities for parasite persistence in the three A. arbustorum populations. We found higher transmission coefficients (β) and larger R₀-values in model 1 than in model 2. Furthermore, the host population with the highest density showed larger R₀-values (16.47-22.59) compared to populations with intermediate (2.71-7.45) or low population density (0.75-4.10). Host threshold population density for parasite persistence ranged from 0.35 to 2.72 snails per m². Our results show that the integration of the disease-relevant biology of the organisms concerned may improve models of host-parasite dynamics.     

Lack of molluscan host diversity and the transmission of an emerging parasitic disease in Bolivia

Fasciolosis is a re-emerging parasitic disease that affects an increasing number of people in developing countries. The most severe endemic affects the Bolivian Altiplano, where the liver fluke (Fasciola hepatica) and its hermaphroditic snail host, Lymnaea truncatula, have been introduced from Europe. To achieve a better understanding of the epidemiological situation and the consequences of the colonization event of this invasive species, genetic analysis of Bolivian snail populations was needed. Here we compare the genetic diversity and population structure of snail samples from the Bolivian Altiplano with samples from the Old World at six polymorphic microsatellite loci. Whereas some variability exists in the snail populations from the Old World, we observe only a single genotype of L. truncatula in the Bolivian Altiplano. We discuss the possible explanations for such a reduction in genetic variability, and, given the high natural parasitism pressures exerted on the snail populations, we discuss the relevance of this result for host-parasite interactions.     

Schistosoma mansoni: Cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata

Sporocysts of Schistosoma mansoni (PR1 strain) survive and grow in Biomphalaria glabrata PR albino strain snails, whereas they are encapsulated and die in B. glabrata 10R2 strain snails. These processes also occur in an in vitro system in which the only living cells are those of sporocysts and snail hemolymph. Hemocytes of the susceptible snail are normally not effective in damaging sporocysts. However, when the encounter occurred in the presence of cell-free plasma from resistant snails, previously impotent hemocytes severely damaged sporocysts in 24 hr. The cytotoxic capacity of resistant strain hemocytes was not altered by plasma from susceptible snails. Furthermore, it was retained even when plasma was replaced by culture medium free of snail components. The nature of the plasma factor(s) which facilitated damage by otherwise impotent hemocytes is discussed, and evidence is evaluated for the hypothesis that snail resistance is dependent upon the specificity of cytophilic factors present both in the plasma and on the hemocyte plasma membranes.     

Evolution of host resistance to parasite infection in the snail–schistosome–human system

The evolutionary strategies that emerge within populations can be dictated by numerous factors, including interactions with other species. In this paper, we explore the consequences of such a scenario using a host-parasite system of human concern. By analyzing the dynamical behaviors of a mathematical model we investigate the evolutionary outcomes resulting from interactions between Schistosoma mansoni and its snail and human hosts. The model includes two types of snail hosts representing resident and mutant types. Using this approach, we focus on establishing evolutionary stable strategies under conditions where snail hosts express different life-histories and when drug treatment is applied to an age-structured population of human hosts. Results from this work demonstrate that the evolutionary trajectories of host-parasite interactions can be varied, and at times, counter-intuitive, based on parasite virulence, host resistance, and drug treatment.     

Host specificity of entomophilic nematodes—A review

Entomophilic nematodes can be biologically manipulated either as biological control agents or as biological insecticide agents. The characteristics, mode of application, and degree of specificity for each of these is considered. The importance of host specificity information for nematode parasites potentially useful in controlling insect pests is emphasized. A general discussion of host specificity and the factors influencing host specificity of entomophilic nematodes is presented.Characteristics of nematodes of the genus Heterotylenchus are discussed while particular emphasis is placed on H. autumnalis, a potentially useful biological control agent of the face fly, Musca autumnalis. Greater detail of the bionomics of this nematode, its attributes and disadvantages as a successful control agent are considered. The factors resulting in host specificity of this parasite, especially host resistance, in Musca domestica, Orthellia caesarion, and Ravinia l'herminieri, are encapsulation and melanization.It is emphasized that biological control workers are working with a dynamic, evolving host-parasite system and that really they are faced with the same problems (resistance of the host and target specificity of the applied material) originally and still confronting the toxicologist and economic entomologist.     

Opportunity or catastrophe? effect of sea salt on host-parasite survival and reproduction

Seawater intrusion associated with decreasing groundwater levels and rising seawater levels may affect freshwater species and their parasites. While brackish water certainly impacts freshwater systems globally, its impact on disease transmission is largely unknown. This study examined the effect of artificial seawater on host-parasite interactions using a freshwater snail host, Biomphalaria alexandrina, and the human trematode parasite Schistosoma mansoni. To evaluate the impact of increasing salinity on disease transmission four variables were analyzed: snail survival, snail reproduction, infection prevalence, and the survival of the parasite infective stage (cercariae). We found a decrease in snail survival, snail egg mass production, and snail infection prevalence as salinity increases. However, cercarial survival peaked at an intermediate salinity value. Our results suggest that seawater intrusion into freshwaters has the potential to decrease schistosome transmission to humans.     

Genotypic vs. condition effects on parasite-driven rare advantage

Models and empirical studies of coevolution assume host resistance and parasite infectivity are genetically based. However, nongenetic physiological or environmental influences could alter host susceptibility even when the relationship is genetically based. In this experiment we examined the influence of host genotype, host condition at the time of infection (age and reproductive status), and their interaction on resistance of the freshwater snail Potamopyrgus antipodarum) to its dominant trematode parasite (Microphallus sp.). We used a laboratory infection experiment of a clonal snail population to determine the susceptibility of juveniles, brooding adult females, and nonbrooding adult females. We found a significant effect of both life-history state and clonal genotype on the prevalence of infection. However, the relative susceptibility of different clonal genotypes was not altered by condition; genotypes that were rare in the natural population were less infected than those that were common for each life-history state. These results suggest that although host condition affects susceptibility, it does not disrupt the specificity of the match between parasites and common clonal genotypes. Hence these findings support the Red Queen hypothesis for the maintenance of sex under genetically based host-parasite interactions.     

HOST-PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME-LAGGED SELECTION IN A NATURAL POPULATION

In theory, parasites can create time-lagged, frequency-dependent selection in their hosts, resulting in oscillatory gene-frequency dynamics in both the host and the parasite (the Red Queen hypothesis). However, oscillatory dynamics have not been observed in natural populations. In the present study, we evaluated the dynamics of asexual clones of a New Zealand snail, Potamopyrgus antipodarum, and its trematode parasites over a five-year period. During the summer of each year, we determined host-clone frequencies in random samples of the snail to track genetic changes in the snail population. Similarly, we monitored changes in the parasite population, focusing on the dominant parasite, Microphallus sp., by calculating the frequency of clones in samples of infected individuals from the same collections. We then compared these results to the results of a computer model that was designed to examine clone frequency dynamics for various levels of parasite virulence. Consistent with these simulations and with ideas regarding dynamic coevolution, parasites responded to common clones in a time-lagged fashion. Finally, in a laboratory experiment, we found that clones that had been rare during the previous five years were significantly less infectible by Microphallus when compared to the common clones. Taken together, these results confirm that rare host genotypes are more likely to escape infection by parasites; they also show that host-parasite interactions produce, in a natural population, some of the dynamics anticipated by the Red Queen hypothesis.     

Schistosoma mansoni: Agglutination of sporocysts,and formation of gels on miracidia transforming in plasma of Biomphalaria glabrata

The resistance or susceptibility of Biomphalaria glabrata strains to strains of Schistosoma mansoni, the human blood fluke, are evidenced by the responses of snail hemocytes to sporocysts of the schistosome, both in vivo and in vitro. It is now reported that living sporocysts of the PR1 strain of S. mansoni agglutinate in the plasma of all tested strains of B. glabrata, in contrast to fixed sporocysts which agglutinate only in plasma from resistant snail strains. The agglutinating activity in resistant plasmas is not divalent cation dependent, and was not inhibited by the 26 carbohydrates and four amino acids tested. In addition, the observation that gelatinous deposits develop on transforming miracidia-sporocysts in B. glabrata plasmas is also reported. Both the agglutination and gel-formation phenomena may facilitate recognition of, and attacks on, sporocysts, thereby contributing to susceptibility and resistance in this host-parasite system.     

Interpopulation differences in hemocyte DNA-comet parameters of snail Lymnaea stagnalis from regions with different environmental loads

Research on hemocytes of snail Lymnaea stagnalis from regions with different environmental loads has been carried out by comet assay. Significant interpopulation differences in hemocyte DNA-comet parameters and sensitivity of hemocyte genetic material to external damaging factors (heavy-metal Sr, in particular) have been revealed by means of software analysis of hemocyte DNA-comet images. Two snail populations are characterized by high genetic identity; therefore, the different proliferative activity in the hemocytes of snail Lymnaea stagnalis from different ecological zones revealed by comet assay may be considered as an indicator of the intensity of damaging effects and environmental quality.     

Long-term population fluctuations of the exotic New Zealand mudsnail <Emphasis Type="Italic">Potamopyrgus antipodarum</Emphasis> and its introduced aporocotylid trematode in northwestern France

Long-term studies of invasive populations are rare, which is unfortunate because important aspects of their dynamics may only be detected over long term. For instance, invasive populations can experience substantial population declines, or even crashes, sometime after their introduction and invasion. Potamopyrgus antipodarum (Caenogastropoda) is a successful invader, and is rarely parasitized in introduced areas. In France, the snail is parasitized as first intermediate host by only one trematode species (Aporocotylid sp. I), native to the snail’s home range, New Zealand. Here, we examined the dynamics of the molluscan assemblage in a French stream on a 14-year interval (2000–2004 and 2009–2013), focusing on this introduced host-parasite association. Overall, P. antipodarum was numerically dominant (90.80%) among molluscs, also including sphaeriid clams (9.12%) and pulmonate snails (0.08%). However, during the last monitoring period, we found a substantial population decline of P. antipodarum, potentially driven by environmental change, such as decreased water temperature and depth, and possibly competitive interactions with sphaeriids, which became numerically dominant (56.34%). P. antipodarum was the only mollusc found infected and only by Aporocotylid sp. I. Interestingly, despite low monthly prevalence (from 0 to 1.52%) and snail host population decline, the P. antipodarum-aporocotylid relationship appeared to be persistent over time.     

Endosymbiont population genomics sheds light on transmission mode,partner specificity,and stability of the scaly-foot snail holobiont

The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host’s cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.Subject terms: Bacterial genomics, Marine microbiology, Symbiosis     

PARTHENOGENESIS IN A FRESHWATER SNAIL: REPRODUCTIVE ASSURANCE VERSUS PARASITIC RELEASE

Two alternative (but not mutually exclusive) hypotheses were contrasted for their abilities to explain the distribution of parthenogenesis in the freshwater snail Potamopyrgus antipodarum: the reproductive assurance hypothesis, which predicts that parthenogenesis will be favored in sparse populations where mates are difficult to find, and the Red Queen hypothesis, which predicts that parthenogenesis will be favored in populations that have a low risk of parasitism. The results were inconsistent with the prediction of the reproductive assurance hypothesis; male frequency was not significantly or positively correlated with snail density. Thus, there was no support for any of the hypotheses for the maintenance of sex that rely on selection for reproductive assurance to explain the distribution of parthenogenesis (e.g., recombinational repair). The results, however, were consistent with the Red Queen hypothesis; male frequency was positively and significantly correlated with the frequency of individuals infected by trematodes. This correlation suggests that parthenogenetic females have replaced sexual females in populations where parasites are rare, and that sexual females have persisted in populations where parasites are common.     

Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses

Snails of the family Lymnaeidae are of great parasitological importance due to the numerous helminth species they transmit, mainly trematodiases (such as fascioliasis) of considerable medical and veterinary impact. The present knowledge of the genetics and host-parasite relationships of this gastropod group is far from adequate. Fascioliasis is caused by two species, Fasciola hepatica and F. gigantica, which, as in the case of other trematodes, show a marked snail host specificity. Many lymnaeid species involved in fascioliasis transmission still show a confused systematic-taxonomic status. The need for tools to distinguish and characterize species and populations of lymnaeids is evident and the present review concerns new molecular tools developed in recent years using nuclear ribosomal DNA sequences. The small subunit or 18S gene and the internal transcribed spacers ITS-2 and ITS-1 are analysed and evaluated as markers for taxon differentiation and relationships within the Lymnaeidae from genus and species levels to subspecies and population levels. rDNA sequence differences and genetic distances, and their value for reconstructing phylogenetic trees using different methods are considered. Nuclear rDNA sequences are appropriate tools on which to base a review of the systematics and taxonomy of the family Lymnaeidae, without excluding other valuable snail characteristics already available. A reconstruction of the lymnaeid system towards a more natural classification will undoubtedly be helpful in understanding parasite transmission and epidemiological features as well the dispersion of an emerging-reemerging disease such as fascioliasis. Nomenclature for nuclear rDNA genotyping in lymnaeids includes the main rDNA sequence regions able to furnish important information on interspecific differentiation and grouping as well as intraspecific variability of lymnaeid species. The composite haplotype code includes the rDNA markers arranged in order according to their well-known usefulness, in its turn related to their respective, more or less rapid evolutionary ratios, to distinguish between different taxonomic levels, from supraspecific taxa to the species level and up to the population level.     

Elevated female fecundity as a possible compensatory mechanism in response to trematode infestation in populations of Littorina saxatilis (Olivi)

Co-evolution between parasites and their hosts may lead to changes in the life-history traits of the host that promote sustainability of their populations despite parasite pressure. Such changes are expected to be especially pronounced in the host-parasite systems where parasites cause complete castration of their hosts. We have studied populations of the rough periwinkle, Littorina saxatilis, infested by castrating trematode species, in order to determine whether high infestation levels are associated with a compensatory increase in host fecundity. To test this hypothesis, we determined female fecundity in populations with trematode prevalence spanning from <1% to 30-75%, and followed long-term changes in female fecundity and trematode infestation in two heavily infested populations of L. saxatilis. The broad-scale geographic analysis of populations with different trematode burdens showed that fecundity of uninfected females is significantly higher in highly infested L. saxatilis populations than in those with low trematode burdens. This is also supported by a comparison of fecundity in two pairs of geographically adjacent populations with contrasting trematode levels, revealing higher fecundity of uninfected females in heavily infested populations. Higher fecundity could be explained by the larger size of uninfected females in some heavily infested populations but not in others. Long-term (15-20 years) intra-population analysis performed in two heavily infested L. saxatilis populations showed that female fecundity increased in parallel with a long-term increase in trematode prevalence from 20% to >75% in one population, but remained high and relatively stable in the second population, reflecting its consistently high trematode prevalence (40-65%). These data support the hypothesis that an increase in female fecundity may be a population compensation mechanism in response to heavy trematode infestation in L. saxatilis and suggest the possible involvement of both natural selection and fast (physiological) regulation mechanisms.     

Comparative Phylogenetic Studies on Schistosoma japonicum and Its Snail Intermediate Host Oncomelania hupensis: Origins,Dispersal and Coevolution

Background

Schistosoma japonicum causes major public health problems in China and the Philippines; this parasite, which is transmitted by freshwater snails of the species Oncomelania hupensis, causes the disease intestinal schistosomiasis in humans and cattle. Researchers working on Schistosoma in Africa have described the relationship between the parasites and their snail intermediate hosts as coevolved or even as an evolutionary arms race. In the present study this hypothesis of coevolution is evaluated for S. japonicum and O. hupensis. The origins and radiation of the snails and the parasite across China, and the taxonomic validity of the sub-species of O. hupensis, are also assessed.

Methodology/Principal Findings

The findings provide no evidence for coevolution between S. japonicum and O. hupensis, and the phylogeographical analysis suggests a heterochronous radiation of the parasites and snails in response to different palaeogeographical and climatic triggers. The results are consistent with a hypothesis of East to West colonisation of China by Oncomelania with a re-invasion of Japan by O. hupensis from China. The Taiwan population of S. japonicum appears to be recently established in comparison with mainland Chinese populations.

Conclusions/Significance

The snail and parasite populations of the western mountain region of China (Yunnan and Sichuan) appear to have been isolated from Southeast Asian populations since the Pleistocene; this has implications for road and rail links being constructed in the region, which will breach biogeographical barriers between China and Southeast Asia. The results also have implications for the spread of S. japonicum. In the absence of coevolution, the parasite may more readily colonise new snail populations to which it is not locally adapted, or even new intermediate host species; this can facilitate its dispersal into new areas. Additional work is required to assess further the risk of spread of S. japonicum.     

Evaluation of mammalian and intermediate host surveillance methods for detecting schistosomiasis reemergence in southwest China

Background

Schistosomiasis has reemerged in China, threatening schistosomiasis elimination efforts. Surveillance methods that can identify locations where schistosomiasis has reemerged are needed to prevent the further spread of infections.

Methods and Principal Findings

We tested humans, cows, water buffalo and the intermediate host snail, Oncomelania hupensis, for Schistosoma japonicum infection, assessed snail densities and extracted regional surveillance records in areas where schistosomiasis reemerged in Sichuan province. We then evaluated the ability of surveillance methods to identify villages where human infections were present. Human infections were detected in 35 of the 53 villages surveyed (infection prevalence: 0 to 43%), including 17 of 28 villages with no prior evidence of reemergence. Bovine infections were detected in 23 villages (infection prevalence: 0 to 65%) and snail infections in one village. Two common surveillance methods, acute schistosomiasis case reports and surveys for S. japonicum-infected snails, grossly underestimated the number of villages where human infections were present (sensitivity 1% and 3%, respectively). Screening bovines for S. japonicum and surveys for the presence of O. hupensis had modest sensitivity (59% and 69% respectively) and specificity (67% and 44%, respectively). Older adults and bovine owners were at elevated risk of infection. Testing only these high-risk human populations yielded sensitivities of 77% and 71%, respectively.

Conclusions

Human and bovine schistosomiasis were widespread in regions where schistosomiasis had reemerged but acute schistosomiasis and S. japonicum-infected snails were rare and, therefore, poor surveillance targets. Until more efficient, sensitive surveillance strategies are developed, direct, targeted parasitological testing of high-risk human populations should be considered to monitor for schistosomiasis reemergence.     

Non-random organization of the Biomphalaria glabrata genome in interphase Bge cells and the spatial repositioning of activated genes in cells co-cultured with Schistosomamansoni

Biomphalaria glabrata is a major intermediate host for the parasitic trematode Schistosoma mansoni, a causative agent of human schistosomiasis. To decipher the molecular basis of this host-parasite interaction, the Bge embryonic cell line provides a unique in vitro model system to assess whether interactions between the snail and parasite affect the cell and genome biology in either organism. The organization of the B. glabrata genome in Bge cells was studied using image analysis through positioning territories of differently sized chromosomes within cell nuclei. The snail chromosome territories are similar in morphology as well as in non-random radial positioning as those found in other derived protostome and deuterostome organisms. Specific monitoring of four gene loci, piwi, BgPrx, actin and ferritin, revealed non-random radial positioning of the genome. This indicates that specific parts of the snail genome reside in reproducible nuclear addresses. To determine whether exposure to parasite is reflected in genome organization, the interphase spatial positioning of genes was assessed after co-culturing Bge cells with either normal or irradiation attenuated miracidia for 30 min to 24 h. The loci of actin and ferritin, genes that are up-regulated in the snail when subjected to infection, were visualized by fluorescence in situ hybridisation (FISH) and their radial nuclear positions i.e. their position in the interphase nucleus with respect to the nuclear edge/envelope, mapped. Interestingly, large scale gene repositioning correlated to temporal kinetics of gene expression levels in Bge cells co-cultured with normal miracidia while irradiated parasites failed to elicit similar gene expression or gene loci repositioning as demonstrated using the ferritin gene. This indicates that normal but not attenuated schistosomes provide stimuli that evoke host responses that are reflected in the host’s nuclear architecture. We believe that this is not only the first time that gene-repositioning studies have been attempted in a mollusc but also demonstrates a parasite influencing the interphase genome organization of its host.