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Host sex and age influence endoparasite burdens in the gray mouse lemur.

Hämäläinen A, Raharivololona B, Ravoniarimbinina P, Kraus C - Front. Zool. (2015)

Bottom Line: With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance.Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness.While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness.

View Article: PubMed Central - PubMed

Affiliation: Department of Sociobiology/Anthropology, Georg-August University of Göttingen, Kellnerweg 6, 37077 Göttingen, Germany ; Behavioral Ecology and Sociobiology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany ; Current address: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9 Canada.

ABSTRACT

Introduction: Immunosenescence (deteriorating immune function at old age) affects humans and laboratory animals, but little is known about immunosenescence in natural populations despite its potential importance for population and disease dynamics and individual fitness. Although life histories and immune system profiles often differ between the sexes, sex-specific effects of aging on health are rarely studied in the wild. Life history theory predicts that due to their shorter lifespan and higher investment into reproduction at the expense of immune defences, males might experience accelerated immunosenescence. We tested this hypothesis by examining sex-specific age trajectories of endoparasite burden (helminth prevalence and morphotype richness measured via fecal egg counts), an indicator of overall health, in wild gray mouse lemurs (Microcebus murinus). To account for potential interactions between seasonality and host sex or age we examined the predictors of parasite burdens separately for the dry and rainy season.

Results: Contrary to the prediction of immunosenescence, parasite prevalence and morphotype richness decreased at old age in the dry season, indicating acquired immunity by older animals. This pattern was primarily caused by within-individual decline in parasite loads rather than the earlier mortality of highly parasitized individuals. With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance. Besides this sex*age interaction, host age was uncorrelated with rainy season parasite loads. Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness.

Conclusions: These results provide rare information about the age-related patterns of health in a wild vertebrate population and suggest improvement rather than senescence in the ability to resist helminth infections at old age. Overall, males appear not to suffer from earlier immunosenescence relative to females. This may partially reflect the earlier mortality of males, which can render senescence difficult to detect. While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness.

No MeSH data available.


Related in: MedlinePlus

Parasite morphotype richness as a function of age in gray mouse lemurs. Predictions for morphotype richness in (a) dry and (b) rainy season shown for males (solid symbols, dashed line) and females (open symbols, solid line). Lines indicate loess smoothers of the age effects (significant decline (in color) in dry season, non-significant (gray-scale) in rainy season) based on the final model in each season (Table 2), and shaded areas indicate 95 % confidence intervals. Morphotype richness was significantly higher in males relative to females in the dry season, whereas no significant sex effect was found in the rainy season. The sex*age interaction was non-significant at the P > 0.05 threshold in both seasons. Both age and morphotype richness are based on discrete measures but jitter was introduced to improve interpretability
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Fig2: Parasite morphotype richness as a function of age in gray mouse lemurs. Predictions for morphotype richness in (a) dry and (b) rainy season shown for males (solid symbols, dashed line) and females (open symbols, solid line). Lines indicate loess smoothers of the age effects (significant decline (in color) in dry season, non-significant (gray-scale) in rainy season) based on the final model in each season (Table 2), and shaded areas indicate 95 % confidence intervals. Morphotype richness was significantly higher in males relative to females in the dry season, whereas no significant sex effect was found in the rainy season. The sex*age interaction was non-significant at the P > 0.05 threshold in both seasons. Both age and morphotype richness are based on discrete measures but jitter was introduced to improve interpretability

Mentions: Parasite morphotype richness ranged from 0 to 4 morphotypes in infected samples. Of the 262 infected samples, 32.8 % (86) contained eggs of more than one morphotype. Based on the final model (Table 2, Fig. 2), morphotype richness declined significantly with age in the dry season but not in the rainy season. Males carried on average twice as many parasite morphotypes as females in the dry season (average for males: 1.2, females: 0.6 morphotypes), whereas no significant sex effect was found in the rainy season (average for both: 0.7 morphotypes). Body mass had a negative effect on morphotype richness in the rainy season, but had the opposite effect in the dry season, likely due to the association of body mass with Hymenolepis infections (Table 2).Fig. 2


Host sex and age influence endoparasite burdens in the gray mouse lemur.

Hämäläinen A, Raharivololona B, Ravoniarimbinina P, Kraus C - Front. Zool. (2015)

Parasite morphotype richness as a function of age in gray mouse lemurs. Predictions for morphotype richness in (a) dry and (b) rainy season shown for males (solid symbols, dashed line) and females (open symbols, solid line). Lines indicate loess smoothers of the age effects (significant decline (in color) in dry season, non-significant (gray-scale) in rainy season) based on the final model in each season (Table 2), and shaded areas indicate 95 % confidence intervals. Morphotype richness was significantly higher in males relative to females in the dry season, whereas no significant sex effect was found in the rainy season. The sex*age interaction was non-significant at the P > 0.05 threshold in both seasons. Both age and morphotype richness are based on discrete measures but jitter was introduced to improve interpretability
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4591582&req=5

Fig2: Parasite morphotype richness as a function of age in gray mouse lemurs. Predictions for morphotype richness in (a) dry and (b) rainy season shown for males (solid symbols, dashed line) and females (open symbols, solid line). Lines indicate loess smoothers of the age effects (significant decline (in color) in dry season, non-significant (gray-scale) in rainy season) based on the final model in each season (Table 2), and shaded areas indicate 95 % confidence intervals. Morphotype richness was significantly higher in males relative to females in the dry season, whereas no significant sex effect was found in the rainy season. The sex*age interaction was non-significant at the P > 0.05 threshold in both seasons. Both age and morphotype richness are based on discrete measures but jitter was introduced to improve interpretability
Mentions: Parasite morphotype richness ranged from 0 to 4 morphotypes in infected samples. Of the 262 infected samples, 32.8 % (86) contained eggs of more than one morphotype. Based on the final model (Table 2, Fig. 2), morphotype richness declined significantly with age in the dry season but not in the rainy season. Males carried on average twice as many parasite morphotypes as females in the dry season (average for males: 1.2, females: 0.6 morphotypes), whereas no significant sex effect was found in the rainy season (average for both: 0.7 morphotypes). Body mass had a negative effect on morphotype richness in the rainy season, but had the opposite effect in the dry season, likely due to the association of body mass with Hymenolepis infections (Table 2).Fig. 2

Bottom Line: With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance.Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness.While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness.

View Article: PubMed Central - PubMed

Affiliation: Department of Sociobiology/Anthropology, Georg-August University of Göttingen, Kellnerweg 6, 37077 Göttingen, Germany ; Behavioral Ecology and Sociobiology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany ; Current address: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9 Canada.

ABSTRACT

Introduction: Immunosenescence (deteriorating immune function at old age) affects humans and laboratory animals, but little is known about immunosenescence in natural populations despite its potential importance for population and disease dynamics and individual fitness. Although life histories and immune system profiles often differ between the sexes, sex-specific effects of aging on health are rarely studied in the wild. Life history theory predicts that due to their shorter lifespan and higher investment into reproduction at the expense of immune defences, males might experience accelerated immunosenescence. We tested this hypothesis by examining sex-specific age trajectories of endoparasite burden (helminth prevalence and morphotype richness measured via fecal egg counts), an indicator of overall health, in wild gray mouse lemurs (Microcebus murinus). To account for potential interactions between seasonality and host sex or age we examined the predictors of parasite burdens separately for the dry and rainy season.

Results: Contrary to the prediction of immunosenescence, parasite prevalence and morphotype richness decreased at old age in the dry season, indicating acquired immunity by older animals. This pattern was primarily caused by within-individual decline in parasite loads rather than the earlier mortality of highly parasitized individuals. With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance. Besides this sex*age interaction, host age was uncorrelated with rainy season parasite loads. Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness.

Conclusions: These results provide rare information about the age-related patterns of health in a wild vertebrate population and suggest improvement rather than senescence in the ability to resist helminth infections at old age. Overall, males appear not to suffer from earlier immunosenescence relative to females. This may partially reflect the earlier mortality of males, which can render senescence difficult to detect. While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness.

No MeSH data available.


Related in: MedlinePlus