Natural Parasite Infection Affects the Tolerance but Not the Response to a Simulated Secondary Parasite Infection

Abstract

Parasites deplete the resources of their host and can consequently affect the investment in competing traits (e.g. reproduction and immune defence). The immunocompetence handicap hypothesis posits that testosterone (T) mediates trade-offs between parasite defence and reproductive investment by suppressing immune function in male vertebrates while more recently a role for glucocorticoids (e.g. cortisol (C)) in resource allocation has been suggested. These hypotheses however, have not always found support in wild animals, possibly because most studies focus on a single parasite species, whereas infections with multiple parasites are the rule in nature. We measured body mass, T- and C-levels of wild male highveld mole-rats (Cryptomys hottentotus pretoriae) naturally uninfected or infected with a cestode (Mathevotaenia sp.) right after capture. Subsequently, we injected animals subcutaneously with a lipopolysaccharide (LPS) to simulate a bacterial infection and recorded changes in body mass, food intake, haematological parameters and hormone levels. As a control, animals were injected with saline. Natural infection neither affected initial body mass nor C-levels, whereas infected males had significantly reduced T-levels. We observed significant reductions in food intake, body mass and T in response to LPS but not saline while C increased. However, this response did not vary with infection status. In contrast, final body mass and some haematological parameters were significantly lowered in infected males. Our results suggest that naturally infected males are able to compensate for resource depletion by physiological adjustments. However, this leaves them less tolerant to the challenges of a secondary infection.

Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

“…Infestation with one parasite can put substantial constraints on the ability of a host to respond to secondary infestations which are likely in the wild due to the ubiquity of more than one parasite species present in natural environments [36]. Similar effects of multiple parasite infestation have also been observed in a closely related mole-rat species, the highveld mole-rat ( Cryptomys hottentotus pretoriae ) [37]. Hence, energy savings obtained in larger groups may have played an important role in overcoming constraints to the evolution of sociality in bathyergids.…”

Trade-offs between immunity and testosterone in male African ground squirrels

“…Although initially proposed by Folstad and Karter (1992) as a negative feedback to the ICHH, this hypothesis has received far less attention and offers an alternative and important mechanism on how the trade-off between reproduction and immunity is modulated. Lutermann et al (2012) found that highveld mole-rats (Cryptomys hottentotus pretoriae) that were naturally infected by cestodes had lower testosterone levels than those who were not infected. They also found that, when faced with an immune challenge through the subcutaneous injection of a lipopolysaccharide (LPS) to stimulate the innate immune system, there was a significant decrease in testosterone levels as well as an increase in cortisol levels.…”

Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta‐analysis

“…Regarding the impact of parasite infection on vertebrate‐host GCs, quantitative methods are required to assess whether parasite‐induced changes in these hormones show general responses in their direction and magnitude across host–parasite associations. It is especially important to establish the broad nature of GC responses in the context of infectious disease dynamics, such as whether they may be expected in host–parasite associations not yet studied, because chronic elevation of GCs could depress immunity and make infected hosts more prone to secondary infections (Lutermann, Bodenstein, & Bennett, ).…”

“…To address such inconsistencies, it is essential to establish whether these discrepancies in GC responses stem from methodological or biological phenomena-questions suitable for meta-anal-infected hosts more prone to secondary infections (Lutermann, Bodenstein, & Bennett, 2012).…”