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Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype.

Wegner KM, Kalbe M, Milinski M, Reusch TB - BMC Evol. Biol. (2008)

Bottom Line: The within family MHC effects were, however, small compared to between family effects, suggesting that other genetic components or non-genetic effects were also important.The correlation between parasite load and mortality that we found at both individual and family level might have appeared only in the extraordinary heatwave of 2003.Due to global warming the frequency of extreme climatic events is predicted to increase, which might intensify costs of parasitism and enhance selection on immune genes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Integrative Biology (IBZ), Experimental Ecology, ETH Zürich, Universitätstrasse 16, CH - 8092 Zürich, Switzerland. mathias.wegner@env.ethz.ch

ABSTRACT

Background: Ecological interaction strength may increase under environmental stress including temperature. How such stress enhances and interacts with parasite selection is almost unknown. We studied the importance of resistance genes of the major histocompatibility complex (MHC) class II in 14 families of three-spined sticklebacks Gasterosteus aculeatus exposed to their natural macroparasites in field enclosures in the extreme summer of 2003.

Results: After a mass die-off during the 2003-European heat wave killing 78% of 277 experimental fish, we found strong differences in survival among and within families. In families with higher average parasite load fewer individuals survived. Multivariate analysis revealed that the composition of the infecting parasite fauna was family specific. Within families, individuals with an intermediate number of MHC class IIB sequence variants survived best and had the lowest parasite load among survivors, suggesting a direct functional link between MHC diversity and fitness. The within family MHC effects were, however, small compared to between family effects, suggesting that other genetic components or non-genetic effects were also important.

Conclusion: The correlation between parasite load and mortality that we found at both individual and family level might have appeared only in the extraordinary heatwave of 2003. Due to global warming the frequency of extreme climatic events is predicted to increase, which might intensify costs of parasitism and enhance selection on immune genes.

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Related in: MedlinePlus

Infection intensities of twelve macroparasite species in nine three-spined stickleback families with at least two survivors. Boxplots show medians (black lines), 25–75% quantiles (boxes), 5–95% quantiles (whiskers) and values outside these ranges (circles). The deviance of the family term from a Generalized Linear Model (GLM) with negative binomial error distributions is given for each species. Bonferroni corrected significant differences among families are indicated based on the family deviance: ***: P < 0.001, **: 0.001 < P < 0.01, ns: not significant.
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Figure 2: Infection intensities of twelve macroparasite species in nine three-spined stickleback families with at least two survivors. Boxplots show medians (black lines), 25–75% quantiles (boxes), 5–95% quantiles (whiskers) and values outside these ranges (circles). The deviance of the family term from a Generalized Linear Model (GLM) with negative binomial error distributions is given for each species. Bonferroni corrected significant differences among families are indicated based on the family deviance: ***: P < 0.001, **: 0.001 < P < 0.01, ns: not significant.

Mentions: We found a wide range of parasite infection intensities for each of the twelve macro-parasite species surveyed in the surviving fish. The parasite species included were the nematodes Anguillicola crassus, Contracaecum spec., Camallanus lacustris and Raphidascaris acus, the digenean trematodes Diplostomum spec., Apatemon cobiditis, Tylodelphis clavata, Cyathocotyle prussica and Echinochasmus spec., the cestodes Valipora campylancristrota and Proteocephalus filicollis, as well as the crustacean Ergasilus spec These parasite species infect various tissues of sticklebacks ranging from inner organs like eyes and muscles, over the digestive tract (gut and gall bladder) to gills and skin [34]. Except for one fish, which did not get infected at all, all other fish got infected by at least 3 different parasite species. This resulted in simultaneous infection of different organs and most likely affected performance of the fish in several ways [34]. The infection patterns of the parasite species formed communities specific to fish families as indicated by the linear discriminant analysis, which could predict fish family with an overall accuracy of 67% (Fig. 1). This proportion of explained variance was significant in Monte Carlo simulations (P = 0.036, 1000 permutations) as well as in conventional MANOVA analysis using the Pillai-Bartlett statistic (Pillai 2.206, approximate F96,328 = 1.301, P = 0.048). The within-family prediction accuracy ranged from 0.333 in family 9 to 1 in family 13. Neither prediction accuracy (χ2d.f. = 1 = 0.195, P = 0.889) nor ordination distance to the respective family mean families (F1,52 = 0.084, P = 0.773) differed significantly between segregating and non-segregating, indicating that variation within segregating families depended only to a minor proportion on different MHC genotypes. Segregating families showed however significantly higher distances from the origin of the ordination (Fig. 1, F1,52 = 4.760, P = 0.034) indicating that the parasite fauna found within segregating families deviated more strongly from the population mean than in non-segregating families. The differences among families observed from the multivariate analysis were also reflected in univariate analysis for each parasite species. Significant differences among families in infection intensities could be detected for five out of the twelve species after sequential Bonferroni correction (Fig. 2). These parasite species also gave the highest canonical weights for the lda ordination (Fig. 1), indicating that family specific infection patterns were mainly driven by these five parasite species.


Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype.

Wegner KM, Kalbe M, Milinski M, Reusch TB - BMC Evol. Biol. (2008)

Infection intensities of twelve macroparasite species in nine three-spined stickleback families with at least two survivors. Boxplots show medians (black lines), 25–75% quantiles (boxes), 5–95% quantiles (whiskers) and values outside these ranges (circles). The deviance of the family term from a Generalized Linear Model (GLM) with negative binomial error distributions is given for each species. Bonferroni corrected significant differences among families are indicated based on the family deviance: ***: P < 0.001, **: 0.001 < P < 0.01, ns: not significant.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2386451&req=5

Figure 2: Infection intensities of twelve macroparasite species in nine three-spined stickleback families with at least two survivors. Boxplots show medians (black lines), 25–75% quantiles (boxes), 5–95% quantiles (whiskers) and values outside these ranges (circles). The deviance of the family term from a Generalized Linear Model (GLM) with negative binomial error distributions is given for each species. Bonferroni corrected significant differences among families are indicated based on the family deviance: ***: P < 0.001, **: 0.001 < P < 0.01, ns: not significant.
Mentions: We found a wide range of parasite infection intensities for each of the twelve macro-parasite species surveyed in the surviving fish. The parasite species included were the nematodes Anguillicola crassus, Contracaecum spec., Camallanus lacustris and Raphidascaris acus, the digenean trematodes Diplostomum spec., Apatemon cobiditis, Tylodelphis clavata, Cyathocotyle prussica and Echinochasmus spec., the cestodes Valipora campylancristrota and Proteocephalus filicollis, as well as the crustacean Ergasilus spec These parasite species infect various tissues of sticklebacks ranging from inner organs like eyes and muscles, over the digestive tract (gut and gall bladder) to gills and skin [34]. Except for one fish, which did not get infected at all, all other fish got infected by at least 3 different parasite species. This resulted in simultaneous infection of different organs and most likely affected performance of the fish in several ways [34]. The infection patterns of the parasite species formed communities specific to fish families as indicated by the linear discriminant analysis, which could predict fish family with an overall accuracy of 67% (Fig. 1). This proportion of explained variance was significant in Monte Carlo simulations (P = 0.036, 1000 permutations) as well as in conventional MANOVA analysis using the Pillai-Bartlett statistic (Pillai 2.206, approximate F96,328 = 1.301, P = 0.048). The within-family prediction accuracy ranged from 0.333 in family 9 to 1 in family 13. Neither prediction accuracy (χ2d.f. = 1 = 0.195, P = 0.889) nor ordination distance to the respective family mean families (F1,52 = 0.084, P = 0.773) differed significantly between segregating and non-segregating, indicating that variation within segregating families depended only to a minor proportion on different MHC genotypes. Segregating families showed however significantly higher distances from the origin of the ordination (Fig. 1, F1,52 = 4.760, P = 0.034) indicating that the parasite fauna found within segregating families deviated more strongly from the population mean than in non-segregating families. The differences among families observed from the multivariate analysis were also reflected in univariate analysis for each parasite species. Significant differences among families in infection intensities could be detected for five out of the twelve species after sequential Bonferroni correction (Fig. 2). These parasite species also gave the highest canonical weights for the lda ordination (Fig. 1), indicating that family specific infection patterns were mainly driven by these five parasite species.

Bottom Line: The within family MHC effects were, however, small compared to between family effects, suggesting that other genetic components or non-genetic effects were also important.The correlation between parasite load and mortality that we found at both individual and family level might have appeared only in the extraordinary heatwave of 2003.Due to global warming the frequency of extreme climatic events is predicted to increase, which might intensify costs of parasitism and enhance selection on immune genes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Integrative Biology (IBZ), Experimental Ecology, ETH Zürich, Universitätstrasse 16, CH - 8092 Zürich, Switzerland. mathias.wegner@env.ethz.ch

ABSTRACT

Background: Ecological interaction strength may increase under environmental stress including temperature. How such stress enhances and interacts with parasite selection is almost unknown. We studied the importance of resistance genes of the major histocompatibility complex (MHC) class II in 14 families of three-spined sticklebacks Gasterosteus aculeatus exposed to their natural macroparasites in field enclosures in the extreme summer of 2003.

Results: After a mass die-off during the 2003-European heat wave killing 78% of 277 experimental fish, we found strong differences in survival among and within families. In families with higher average parasite load fewer individuals survived. Multivariate analysis revealed that the composition of the infecting parasite fauna was family specific. Within families, individuals with an intermediate number of MHC class IIB sequence variants survived best and had the lowest parasite load among survivors, suggesting a direct functional link between MHC diversity and fitness. The within family MHC effects were, however, small compared to between family effects, suggesting that other genetic components or non-genetic effects were also important.

Conclusion: The correlation between parasite load and mortality that we found at both individual and family level might have appeared only in the extraordinary heatwave of 2003. Due to global warming the frequency of extreme climatic events is predicted to increase, which might intensify costs of parasitism and enhance selection on immune genes.

Show MeSH
Related in: MedlinePlus