Most cited article - PubMed ID 17557157
Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish
Fish-borne zoonoses are emerging worldwide, and although most human cases remain confined to tropical regions, particularly Southeast and East Asia, a few cases have been reported in Europe. This review summarizes published and new data on the life cycle of Metagonimus romanicus (misidentified as M. yokogawai, a human pathogen common in East Asia), a heterophyid trematode and one of the potentially fish-borne parasites in Europe. Metagonimus romanicus is distributed from the middle Danube in Central Europe (Slovakia) to eastern Ukraine (including the rivers of the Black Sea basin). Its distribution area coincides with that of its first intermediate hosts, the melanopsid snails Microcolpia daudebartii acicularis and Esperiana esperi. While M. romanicus most likely has a strict specificity for its first snail hosts, metacercariae are generalists and have been detected in over 50 freshwater fish species from 18 families, especially leuciscids. Despite its wide distribution and frequent occurrence in freshwater fish, the zoonotic potential of M. romanicus appears to be low. This is probably due to the exclusive localization of the metacercariae in the fish scales rather than musculature, as well as the rare consumption of raw or undercooked fish in Europe. However, some risk remains and a small number of undiagnosed human infections due to accidental ingestion of scales during the preparation and cleaning of fish cannot be ruled out.
- Keywords
- Cercariae, Europe, Fish, Freshwater, Metacercariae, Snails,
- Publication type
- Journal Article MeSH
BACKGROUND: Recently, human intervention enabled the introduction of Barbus barbus from the Rhône River basin into the Barbus meridionalis habitats of the Argens River. After an introduction event, parasite loss and lower infection can be expected in non-native hosts in contrast to native species. Still, native species might be endangered by hybridization with the incomer and the introduction of novel parasite species. In our study, we aimed to examine metazoan parasite communities in Barbus spp. populations in France, with a special emphasis on the potential threat posed by the introduction of novel parasite species by invasive B. barbus to local B. meridionalis. METHODS: Metazoan parasite communities were examined in B. barbus, B. meridionalis and their hybrids in three river basins in France. Microsatellites were used for the species identification of individual fish. Parasite abundance, prevalence, and species richness were compared. Effects of different factors on parasite infection levels and species richness were tested using GLM. RESULTS: Metazoan parasites followed the expansion range of B. barbus and confirmed its introduction into the Argens River. Here, the significantly lower parasite number and lower levels of infection found in B. barbus in contrast to B. barbus from the Rhône River supports the enemy release hypothesis. Barbus barbus × B. meridionalis hybridization in the Argens River basin was confirmed using both microsatellites and metazoan parasites, as hybrids were infected by parasites of both parental taxa. Trend towards higher parasite diversity in hybrids when compared to parental taxa, and similarity between parasite communities from the Barbus hybrid zone suggest that hybrids might represent "bridges" for parasite infection between B. barbus and B. meridionalis. Risk of parasite transmission from less parasitized B. barbus to more parasitized B. meridionalis indicated from our study in the Argens River might be enhanced in time as higher infection levels in B. barbus from the Rhône River were revealed. Hybrid susceptibility to metazoan parasites varied among the populations and is probably driven by host-parasite interactions and environmental forces. CONCLUSIONS: Scientific attention should be paid to the threatened status of the endemic B. meridionalis, which is endangered by hybridization with the invasive B. barbus, i.e. by genetic introgression and parasite transmission.
- Keywords
- Biological invasion, Cyprinid fish, Hybridization, Metazoan parasite communities,
- MeSH
- Biodiversity * MeSH
- Chimera classification genetics growth & development parasitology MeSH
- Cyprinidae classification genetics growth & development parasitology MeSH
- Microsatellite Repeats MeSH
- Parasite Load MeSH
- Parasites classification isolation & purification MeSH
- Rivers MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- France MeSH
The genes of major histocompatibility complex (MHC) provide an excellent opportunity to study host-parasite relationships because they are expected to evolve in response to parasites and variation in parasite communities. In this study, we investigated the potential role of parasite-mediated selection acting on MHC class IIB (DAB) genes in European chub (Squalius cephalus) natural populations. We found significant differences between populations in metazoan parasites, neutral and adaptive genetic diversities. The analyses based on pairwise data revealed that populations with dissimilar MHC allelic profiles were geographically distant populations with significantly different diversity in microsatellites and a dissimilar composition of parasite communities. The results from the generalized estimating equations method (GEE) on the level of individuals revealed that metazoan parasite load in European chub was influenced by the diversity of DAB alleles as well as by the diversity of neutral genetic markers and host traits reflecting condition and immunocompetence. The multivariate co-inertia analysis showed specific associations between DAB alleles and parasite species. DAB1-like alleles were more involved in associations with ectoparasites, while DAB3-like alleles were positively associated with endoparasites which could suggest potential differences between DAB genes caused by different selection pressure. Our study revealed that parasite-mediated selection is not the only variable affecting MHC diversity in European chub; however, we strongly support the role of neutral processes as the main driver of DAB diversity across populations. In addition, our study contributes to the understanding of the evolution of MHC genes in wild living fish.
- Keywords
- Genetic diversity, Major histocompatibility complex, Metazoan parasites, Microsatellites, Parasite-driven balancing selection, Phylogeography,
- MeSH
- Alleles MeSH
- Cyprinidae genetics MeSH
- Animals, Wild MeSH
- Genetic Variation * MeSH
- Major Histocompatibility Complex genetics MeSH
- Host-Parasite Interactions MeSH
- Microsatellite Repeats genetics MeSH
- Fish Diseases parasitology MeSH
- Parasitic Diseases, Animal epidemiology genetics parasitology MeSH
- Parasites MeSH
- Selection, Genetic * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe epidemiology MeSH
BACKGROUND: The basic function of the immune system is to protect an organism against infection in order to minimize the fitness costs of being infected. According to life-history theory, energy resources are in a trade-off between the costly demands of immunity and other physiological demands. Concerning fish, both physiology and immunity are influenced by seasonal changes (i.e. temporal variation) associated to the changes of abiotic factors (such as primarily water temperature) and interactions with pathogens and parasites. In this study, we investigated the potential associations between the physiology and immunocompetence of common carp (Cyprinus carpio) collected during five different periods of a given year. Our sampling included the periods with temporal variability and thus, it presented a different level in exposure to parasites. We analyzed which of two factors, seasonality or parasitism, had the strongest impact on changes in fish physiology and immunity. RESULTS: We found that seasonal changes play a key role in affecting the analyzed measurements of physiology, immunity and parasitism. The correlation analysis revealed the relationships between the measures of overall host physiology, immunity and parasite load when temporal variability effect was removed. When analyzing separately parasite groups with different life-strategies, we found that fish with a worse condition status were infected more by monogeneans, representing the most abundant parasite group. The high infection by cestodes seems to activate the phagocytes. A weak relationship was found between spleen size and abundance of trematodes when taking into account seasonal changes. CONCLUSIONS: Even if no direct trade-off between the measures of host immunity and physiology was confirmed when taking into account the seasonality, it seems that seasonal variability affects host immunity and physiology through energy allocation in a trade-off between life important functions, especially reproduction and fish condition. Host immunity measures were not found to be in a trade-off with the investigated physiological traits or functions, but we confirmed the immunosuppressive role of 11-ketotestosterone on fish immunity measured by complement activity. We suggest that the different parasite life-strategies influence different aspects of host physiology and activate the different immunity pathways.
- MeSH
- Immunoglobulin M blood MeSH
- Carps immunology parasitology physiology MeSH
- Complement System Proteins immunology MeSH
- Leukocytes immunology MeSH
- Parasitic Diseases, Animal immunology MeSH
- Parasites immunology MeSH
- Seasons MeSH
- Reproduction MeSH
- Spleen immunology MeSH
- Body Weight MeSH
- Testosterone analogs & derivatives blood MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- 11-ketotestosterone MeSH Browser
- Immunoglobulin M MeSH
- Complement System Proteins MeSH
- Testosterone MeSH
Each organism has the limited resources of energy that is distributed among important life traits. A trade-off between immune response and other physiological demands of organism especially costly reproduction is expected. Leuciscus cephalus, the cyprinid fish, was investigated during three periods varying in reproductive investment, that is, before-breeding, breeding, and after-breeding periods. We tested whether a potentially limited investment in immunity during the breeding is associated with higher susceptibility to the metazoan parasites. Following the immunocompetence handicap and sperm protection hypotheses, males expressing more elaborated sexual ornamentation should produce better quality sperm and be more parasitized. We found that reproductive investments in fish play an important role for energy allocation into somatic condition, immunity, and reproduction. The immune parameters including respiratory burst and leukocyte count were higher in breeding; however, parasite species richness and abundance appeared low. Males investing more in spawning tubercles reached high spermatocrite and were more parasitized by digeneans.
- MeSH
- Principal Component Analysis MeSH
- Analysis of Variance MeSH
- Cyprinidae immunology parasitology physiology MeSH
- Host-Parasite Interactions MeSH
- Fish Diseases blood immunology parasitology MeSH
- Parasitic Diseases, Animal blood immunology parasitology MeSH
- Leukocyte Count MeSH
- Reproduction immunology physiology MeSH
- Body Weights and Measures MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: The main prediction of life-history theory is that optimal energy allocated among the traits is related to the growth, maintenance and survival. It is hypothesized that the optimal resource allocated to immune function, which generates resistance towards parasites and reduce the fitness losses caused by parasitism, is depending on other requirements for energetic resource and the benefits associated with them. The aims of this study are to investigate in a comparative way (1) how parasitism is related to fish life history traits (fecundity, longevity, mortality), (2) whether there is a trade-off between reproduction and immune investments in fish females (i.e. energetic hypothesis) and in males (i.e. immunohandicap hypothesis), (3) whether parasitism influences host immunity (spleen size) and reproduction (gonad size) in females and males. RESULTS: Data on metazoan parasites of 23 cyprinid fish species from Central Europe were used for the analyses as well as new data collected from a field study. Ectoparasite species richness was negatively correlated with the fish mortality estimated by the k-value and positively correlated with fish body size, suggesting that parasite diversity increases with fish longevity. A negative relationship between spleen size and gonad size, controlling for fish body size, was found in females but not in males. Moreover, parasite abundance was positively correlated with fish spleen size and negatively with fish gonad size in females. CONCLUSION: The comparative analyses using cyprinid fish species demonstrated that natural mortality could be considered as a factor contributing to the variability of parasite species richness and moreover, parasite species benefit from long-lived fish. The results obtained from the analyses investigating the potential trade-off between reproduction and immunity could be interpreted as an energetic trade-off between female reproduction and immune function. The lack of negative relationship between gonad size and spleen size in males did not support our prediction based on the immunohandicap hypothesis.
- MeSH
- Helminths growth & development MeSH
- Gonads growth & development parasitology MeSH
- Fishes growth & development immunology parasitology MeSH
- Spleen growth & development parasitology MeSH
- Organ Size MeSH
- Body Size MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH