Limits...
Markedly Elevated Antibody Responses in Wild versus Captive Spotted Hyenas Show that Environmental and Ecological Factors Are Important Modulators of Immunity.

Flies AS, Mansfield LS, Grant CK, Weldele ML, Holekamp KE - PLoS ONE (2015)

Bottom Line: Wild spotted hyenas (Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species.Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations.The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

View Article: PubMed Central - PubMed

Affiliation: Menzies Research Institute Tasmania, University of Tasmania, Hobart, TAS, Australia; Department of Zoology, Michigan State University, East Lansing, MI, United States of America; Interdisciplinary program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI, United States of America; Department of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia.

ABSTRACT
Evolutionary processes have shaped the vertebrate immune system over time, but proximal mechanisms control the onset, duration, and intensity of immune responses. Based on testing of the hygiene hypothesis, it is now well known that microbial exposure is important for proper development and regulation of the immune system. However, few studies have examined the differences between wild animals in their natural environments, in which they are typically exposed to a wide array of potential pathogens, and their conspecifics living in captivity. Wild spotted hyenas (Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species. Here we assessed differences in immune defenses between wild spotted hyenas that inhabit their natural savanna environment and captive hyenas that inhabit a captive environment where pathogen control programs are implemented. Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations. Our results show that wild hyenas have significantly higher serum antibody concentrations, including total IgG and IgM, natural antibodies, and autoantibodies than do captive hyenas; there was no difference in the bacterial killing capacity of sera collected from captive and wild hyenas. The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

No MeSH data available.


Related in: MedlinePlus

Relative concentrations of anti-KLH natural antibodies.Anti-KLH natural IgG (A) is significantly higher in wild hyenas (n = 14) than in captive hyenas (n = 11), but there is no difference in anti-KLH natural IgM (B) between wild (n = 14) captive (n = 11) hyenas. Females are indicated by open circles and males by filled circles. *** p < 0.001.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4621877&req=5

pone.0137679.g003: Relative concentrations of anti-KLH natural antibodies.Anti-KLH natural IgG (A) is significantly higher in wild hyenas (n = 14) than in captive hyenas (n = 11), but there is no difference in anti-KLH natural IgM (B) between wild (n = 14) captive (n = 11) hyenas. Females are indicated by open circles and males by filled circles. *** p < 0.001.

Mentions: We measured natural antibodies to KLH in sera from 11 captive hyenas and 14 wild hyenas. As with total IgG, there was again only a single model with Δ AICc < 2, however, this time the model included captivity status, sex, and an interaction between captivity status and sex. Wild hyenas had significantly higher concentrations of anti-KLH nIgG than captive hyenas (p < 0.001) (Fig 3A). There was also a significant interaction between captivity status and sex (p = 0.003), with all wild female hyenas having higher concentrations of anti-KLH nIgG than wild male hyenas (Fig 3A). The weighted averages from the four anti-KLH nIgM models with Δ AICc < 2 suggest that there was no statistically significant difference (p = 0.116) between anti-KLH nIgM concentrations in wild hyenas than captive hyenas (Fig 3B). a marginally non-significant interaction between sex and age (p = 0.051), with anti-KLH nIgM decreasing with age in females. (See S2 Table for full list of effect sizes, confidence intervals, and p-values for the analysis of natural anti-KLH nIgG and nIgM)


Markedly Elevated Antibody Responses in Wild versus Captive Spotted Hyenas Show that Environmental and Ecological Factors Are Important Modulators of Immunity.

Flies AS, Mansfield LS, Grant CK, Weldele ML, Holekamp KE - PLoS ONE (2015)

Relative concentrations of anti-KLH natural antibodies.Anti-KLH natural IgG (A) is significantly higher in wild hyenas (n = 14) than in captive hyenas (n = 11), but there is no difference in anti-KLH natural IgM (B) between wild (n = 14) captive (n = 11) hyenas. Females are indicated by open circles and males by filled circles. *** p < 0.001.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4621877&req=5

pone.0137679.g003: Relative concentrations of anti-KLH natural antibodies.Anti-KLH natural IgG (A) is significantly higher in wild hyenas (n = 14) than in captive hyenas (n = 11), but there is no difference in anti-KLH natural IgM (B) between wild (n = 14) captive (n = 11) hyenas. Females are indicated by open circles and males by filled circles. *** p < 0.001.
Mentions: We measured natural antibodies to KLH in sera from 11 captive hyenas and 14 wild hyenas. As with total IgG, there was again only a single model with Δ AICc < 2, however, this time the model included captivity status, sex, and an interaction between captivity status and sex. Wild hyenas had significantly higher concentrations of anti-KLH nIgG than captive hyenas (p < 0.001) (Fig 3A). There was also a significant interaction between captivity status and sex (p = 0.003), with all wild female hyenas having higher concentrations of anti-KLH nIgG than wild male hyenas (Fig 3A). The weighted averages from the four anti-KLH nIgM models with Δ AICc < 2 suggest that there was no statistically significant difference (p = 0.116) between anti-KLH nIgM concentrations in wild hyenas than captive hyenas (Fig 3B). a marginally non-significant interaction between sex and age (p = 0.051), with anti-KLH nIgM decreasing with age in females. (See S2 Table for full list of effect sizes, confidence intervals, and p-values for the analysis of natural anti-KLH nIgG and nIgM)

Bottom Line: Wild spotted hyenas (Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species.Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations.The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

View Article: PubMed Central - PubMed

Affiliation: Menzies Research Institute Tasmania, University of Tasmania, Hobart, TAS, Australia; Department of Zoology, Michigan State University, East Lansing, MI, United States of America; Interdisciplinary program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI, United States of America; Department of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia.

ABSTRACT
Evolutionary processes have shaped the vertebrate immune system over time, but proximal mechanisms control the onset, duration, and intensity of immune responses. Based on testing of the hygiene hypothesis, it is now well known that microbial exposure is important for proper development and regulation of the immune system. However, few studies have examined the differences between wild animals in their natural environments, in which they are typically exposed to a wide array of potential pathogens, and their conspecifics living in captivity. Wild spotted hyenas (Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species. Here we assessed differences in immune defenses between wild spotted hyenas that inhabit their natural savanna environment and captive hyenas that inhabit a captive environment where pathogen control programs are implemented. Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations. Our results show that wild hyenas have significantly higher serum antibody concentrations, including total IgG and IgM, natural antibodies, and autoantibodies than do captive hyenas; there was no difference in the bacterial killing capacity of sera collected from captive and wild hyenas. The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

No MeSH data available.


Related in: MedlinePlus