The immune system is one of the most complex physiological systems in animals. In light of this complexity, immunologists have traditionally tried to eliminate genetic and environmental variation by using highly inbred rodents reared in highly controlled and relatively hygienic environments. However, the immune systems of animals evolved in unsanitary, stochastic environments. Furthermore, socio-ecological variables affect the development and activation of immune defenses within an individual, resulting in a high degree of variation in immune defenses even among individuals with similar genetic backgrounds. The conventional immunology approach of eliminating these variables allows us to answer some questions with great clarity, but a fruitful complement is to quantify how the social and ecological factors impact the immune function of animals living in their natural, pathogen-rich environments. Spotted hyenas (Crocuta crocuta) have recently descended from carrion feeding ancestors, and they routinely survive infection by a plethora of deadly pathogens, such rabies, distemper virus, and anthrax. Additionally, spotted hyenas live in large, complex societies, called clans, in which the effects of social rank pervade many aspects of hyena biology. High-ranking hyenas have priority of access to food resources, and rank is positively correlated with fitness. However, very little research has been done to understand basic immune function in spotted hyenas or how socio-ecological variables such as rank can affect immune function. Here we addressed three primary questions. First, why do spotted hyenas rarely die from infectious disease? Second, is the spotted hyena immune system fundamentally different from that of other mammals? Third, how do socio-ecological variables affect immune function in spotted hyenas. Here we show that two primary components of the hyena immune system, immunoglobulins and toll-like receptors (TLRs), are similar to those in domestic cats (Felis catus), the closest relative of hyenas that has been studied in depth immunologically. The structure and molecular weights of hyena immunoglobulins are similar to those of cats, and the dynamics of the hyena antibody response to immunization also follow the standard pattern observed in cats. DNA sequencing of hyena toll-like receptors revealed more than 90% sequence similarity between hyenas and cats. Given the importance of rank in spotted hyena clans, we investigated the effects of social rank on immune function in wild hyenas. Social rank is significantly correlated with serum bacterial killing capacity and total IgM. Additionally, serum bacterial killing capacity and total IgM are lower in lactating than in pregnant females. The higher levels of immune defenses in high-ranking females than in low-ranking females, and the reduced immune defenses observed during the energy costly period of lactation, suggests that immune defenses may be traded-off with other physiological systems. Furthermore, we found that bacterial killing capacity is a significant predictor of annual reproductive success in wild female hyenas. Finally, we assessed the differences in immune function between wild hyenas inhabiting a relatively pathogen-rich environment and captive hyenas in a relatively hygienic environment. Here we show that free-living hyenas generally had higher levels of immune defenses than captive hyenas. The lack of mortality from infectious disease in the wild hyenas suggests that their immune defenses are robust, and that pathogen exposure may be important for the development of the immune system, as suggested by the hygiene hypothesis.
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