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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

Apparent survival of gray mouse lemurs is not significantly influenced by morphotype richness (Table 4). Apparent survival to next season (~6 months, based on capture data) as a function of parasite infections in the 2010 dry season (open brown triangle & solid line), 2012 dry season (open orange circles & dotted line) and the 2012 rainy season (filled green circles & dashed line). Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) and season-specific loess-smoothed prediction lines and 95 % confidence bands based on a binomial GLM
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Fig3: Apparent survival of gray mouse lemurs is not significantly influenced by morphotype richness (Table 4). Apparent survival to next season (~6 months, based on capture data) as a function of parasite infections in the 2010 dry season (open brown triangle & solid line), 2012 dry season (open orange circles & dotted line) and the 2012 rainy season (filled green circles & dashed line). Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) and season-specific loess-smoothed prediction lines and 95 % confidence bands based on a binomial GLM

Mentions: The average apparent survival probability to next season (i.e. ~6 months, based on capture data) of individuals infected by one or more parasite morphotypes was 0.47 ± 0.10 in the dry season and 0.66 ± 0.11 in the rainy season, whereas for uninfected individuals the same survival probabilities were 0.55 ± 0.10 and 0.72 ± 0.10, respectively. This tentatively suggests that individuals infected with gastrointestinal parasites may experience a slightly lower survival probability, but this difference is not statistically significant (Table 4). Within infected animals, morphotype richness had no influence on apparent survival, as the survival probability of individuals excreting one morphotype was 0.57 ± 0.09 relative to 0.57 ± 0.16 for those individuals carrying 3-4 different morphotypes (Fig. 3, Table 4).Table 4


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

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

Apparent survival of gray mouse lemurs is not significantly influenced by morphotype richness (Table 4). Apparent survival to next season (~6 months, based on capture data) as a function of parasite infections in the 2010 dry season (open brown triangle & solid line), 2012 dry season (open orange circles & dotted line) and the 2012 rainy season (filled green circles & dashed line). Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) and season-specific loess-smoothed prediction lines and 95 % confidence bands based on a binomial GLM
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig3: Apparent survival of gray mouse lemurs is not significantly influenced by morphotype richness (Table 4). Apparent survival to next season (~6 months, based on capture data) as a function of parasite infections in the 2010 dry season (open brown triangle & solid line), 2012 dry season (open orange circles & dotted line) and the 2012 rainy season (filled green circles & dashed line). Shown are all data points (with jitter introduced to the discrete variables for ease of interpretation) and season-specific loess-smoothed prediction lines and 95 % confidence bands based on a binomial GLM
Mentions: The average apparent survival probability to next season (i.e. ~6 months, based on capture data) of individuals infected by one or more parasite morphotypes was 0.47 ± 0.10 in the dry season and 0.66 ± 0.11 in the rainy season, whereas for uninfected individuals the same survival probabilities were 0.55 ± 0.10 and 0.72 ± 0.10, respectively. This tentatively suggests that individuals infected with gastrointestinal parasites may experience a slightly lower survival probability, but this difference is not statistically significant (Table 4). Within infected animals, morphotype richness had no influence on apparent survival, as the survival probability of individuals excreting one morphotype was 0.57 ± 0.09 relative to 0.57 ± 0.16 for those individuals carrying 3-4 different morphotypes (Fig. 3, Table 4).Table 4

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