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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

Seasonal prevalence of the three common parasite egg morphotypes. Prevalences (probability of infection) shown for Subulura (a) dry season and (d) rainy season; Trichuris (b) dry and (e) rainy season; and Hymenolepis (c) dry and (f) rainy season in samples from gray mouse lemurs in Kirindy forest. Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) for males (solid symbol) and females (open symbol), and loess-smoothed prediction lines and 95 % confidence bands for age effects for males (dashed line) and females (solid line). Significant age effects (a and c, trajectories not significantly different for the sexes), and a significant age*sex interaction (f) shown with colored confidence bands, non-significant relationships with gray confidence bands. See text and Table 2 for details
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Fig1: Seasonal prevalence of the three common parasite egg morphotypes. Prevalences (probability of infection) shown for Subulura (a) dry season and (d) rainy season; Trichuris (b) dry and (e) rainy season; and Hymenolepis (c) dry and (f) rainy season in samples from gray mouse lemurs in Kirindy forest. Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) for males (solid symbol) and females (open symbol), and loess-smoothed prediction lines and 95 % confidence bands for age effects for males (dashed line) and females (solid line). Significant age effects (a and c, trajectories not significantly different for the sexes), and a significant age*sex interaction (f) shown with colored confidence bands, non-significant relationships with gray confidence bands. See text and Table 2 for details

Mentions: Contrary to our prediction of immunosenescence, host age was negatively associated with the prevalence of eggs of the Subulura and Hymenolepis families, but not Trichuris, in the dry season (Table 2, Fig. 1). More of these parasites were found in males and in young individuals relative to females and older individuals. In line with our prediction of earlier immunosenescence in males, a significant sex*age interaction was found for Hymenolepis in the rainy season with older males exhibiting higher infection rates, but no other models indicated a significant effect of the sex*age interaction term (Table 2, Fig. 1). Trichuris-type eggs were found in the rainy season only in samples collected in year 2012 from female hosts, with all other samples being negative. No age or sex effects were found in the rainy season for Subulura.Table 2


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

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

Seasonal prevalence of the three common parasite egg morphotypes. Prevalences (probability of infection) shown for Subulura (a) dry season and (d) rainy season; Trichuris (b) dry and (e) rainy season; and Hymenolepis (c) dry and (f) rainy season in samples from gray mouse lemurs in Kirindy forest. Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) for males (solid symbol) and females (open symbol), and loess-smoothed prediction lines and 95 % confidence bands for age effects for males (dashed line) and females (solid line). Significant age effects (a and c, trajectories not significantly different for the sexes), and a significant age*sex interaction (f) shown with colored confidence bands, non-significant relationships with gray confidence bands. See text and Table 2 for details
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Seasonal prevalence of the three common parasite egg morphotypes. Prevalences (probability of infection) shown for Subulura (a) dry season and (d) rainy season; Trichuris (b) dry and (e) rainy season; and Hymenolepis (c) dry and (f) rainy season in samples from gray mouse lemurs in Kirindy forest. Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) for males (solid symbol) and females (open symbol), and loess-smoothed prediction lines and 95 % confidence bands for age effects for males (dashed line) and females (solid line). Significant age effects (a and c, trajectories not significantly different for the sexes), and a significant age*sex interaction (f) shown with colored confidence bands, non-significant relationships with gray confidence bands. See text and Table 2 for details
Mentions: Contrary to our prediction of immunosenescence, host age was negatively associated with the prevalence of eggs of the Subulura and Hymenolepis families, but not Trichuris, in the dry season (Table 2, Fig. 1). More of these parasites were found in males and in young individuals relative to females and older individuals. In line with our prediction of earlier immunosenescence in males, a significant sex*age interaction was found for Hymenolepis in the rainy season with older males exhibiting higher infection rates, but no other models indicated a significant effect of the sex*age interaction term (Table 2, Fig. 1). Trichuris-type eggs were found in the rainy season only in samples collected in year 2012 from female hosts, with all other samples being negative. No age or sex effects were found in the rainy season for Subulura.Table 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