RESUMEN
When animals are faced with a life-threatening challenge, they mount an organism-wide response (i.e. Plan A). For example, both the stress response (i.e. fight-or-flight) and the immune response recruit molecular resources from other body tissues, and induce physiological changes that optimize the body for defense. However, pathogens and predators often co-occur. Animals that can optimize responses for a dual challenge, i.e. simultaneous predator and pathogen attacks, will have a selective advantage. Responses to a combined predator and pathogen attack have not been well studied, but this paper summarizes the existing literature in insects. The response to dual challenges (i.e. Plan B) results in a suite of physiological changes that are different from either the stress response or the immune response, and is not a simple summation of the two. It is also not a straight-forward trade-off of one response against the other. The response to a dual challenge (i.e. Plan B) appears to resolve physiological trade-offs between the stress and immune responses, and reconfigures both responses to provide the best overall defense. However, the dual response appears to be more costly than either response occurring singly, resulting in greater damage from oxidative stress, reduced growth rate, and increased mortality.
Asunto(s)
Insectos/fisiología , Estrés Fisiológico , Animales , Interacciones Huésped-Patógeno , Insectos/microbiología , Conducta PredatoriaRESUMEN
Immune-nociceptor connections are found in animals across phyla. Local inflammation and/or damage results in increased nociceptive sensitivity of the affected area. However, in mammals, immune responses far from peripheral nociceptors, such as immune responses in the gut, produce a general increase in peripheral nociceptive sensitivity. This phenomenon has not, to our knowledge, been found in other animal groups. We found that consuming heat-killed pathogens reduced the tactile force needed to induce a defensive strike in the caterpillar Manduca sexta. This increase in the nociceptive sensitivity of the body wall is probably part of the reconfiguration of behaviour and physiology that occurs during an immune response (e.g. sickness behaviour). This increase may help enhance anti-predator behaviour as molecular resources are shifted towards the immune system. This article is part of the Theo Murphy meeting issue 'Evolution of mechanisms and behaviour important for pain'.
Asunto(s)
Manduca/inmunología , Nocicepción , Animales , Tracto Gastrointestinal/inmunología , Larva/crecimiento & desarrollo , Larva/inmunología , Manduca/crecimiento & desarrolloRESUMEN
Mounting an immune response consumes resources, which should lead to increased feeding. However, activating the immune system reduces feeding (i.e. illness-induced anorexia) in both vertebrates and invertebrates, suggesting that it may be beneficial. We suggest that illness-induced anorexia may be an adaptive response to conflicts between immune defense and food detoxification. We found that activating an immune response in the caterpillar Manduca sexta increased its susceptibility to the toxin permethrin. Conversely, a sublethal dose of permethrin reduced resistance to the bacterium Serratia marcescens, demonstrating a negative interaction between detoxification and immune defense. Immune system activation and toxin challenge each depleted the amount of glutathione in the hemolymph. Increasing glutathione concentration in the hemolymph increased survival for both toxin- and immune+toxin-challenged groups. The results of this rescue experiment suggest that decreased glutathione availability, such as occurs during an immune response, impairs detoxification. We also found that the expression of some detoxification genes were not upregulated during a combined immune-toxin challenge, although they were when animals received a toxin challenge alone. These results suggest that immune defense reduces food detoxification capacity. Illness-induced anorexia may protect animals by decreasing exposure to food toxins when detoxification is impaired.
Asunto(s)
Antibiosis , Inmunidad Innata , Insecticidas/toxicidad , Manduca/inmunología , Manduca/microbiología , Permetrina/toxicidad , Serratia marcescens/fisiología , Animales , Ingestión de Alimentos , Larva/inmunología , Larva/microbiología , Manduca/crecimiento & desarrollo , Fase I de la Desintoxicación MetabólicaRESUMEN
The classic biomedical view is that stress hormone effects on the immune system are largely pathological, especially if the stress is chronic. However, more recent interpretations have focused on the potential adaptive function of these effects. This paper examines stress response-immune system interactions from a physiological network perspective, using insects because of their simpler physiology. For example, stress hormones can reduce disease resistance, yet activating an immune response results in the release of stress hormones in both vertebrates and invertebrates. From a network perspective, this phenomenon is consistent with the 'sharing' of the energy-releasing ability of stress hormones by both the stress response and the immune system. Stress-induced immunosuppression is consistent with the stress response 'borrowing' molecular components from the immune system to increase the capacity of stress-relevant physiological processes (i.e. a trade off). The insect stress hormones octopamine and adipokinetic hormone can also 'reconfigure' the immune system to help compensate for the loss of some of the immune system's molecular resources (e.g. apolipophorin III). This view helps explain seemingly maladaptive interactions between the stress response and immune system. The adaptiveness of stress hormone effects on individual immune components may be apparent only from the perspective of the whole organism. These broad principles will apply to both vertebrates and invertebrates.
Asunto(s)
Sistema Inmunológico/fisiología , Estrés Fisiológico/inmunología , Animales , Apolipoproteínas/metabolismo , Hormonas de Insectos/metabolismo , Insectos , Octopamina/metabolismo , Oligopéptidos/metabolismo , Ácido Pirrolidona Carboxílico/análogos & derivados , Ácido Pirrolidona Carboxílico/metabolismoRESUMEN
Immune activation alters behaviour (i.e. sickness behaviour) in animals across phyla and is thought to aid recovery from infection. Hypotheses regarding the adaptive function of different sickness behaviours (e.g. decreased movement and appetite) include the energy conservation and predator avoidance hypotheses. These hypotheses were originally developed for mammals (e.g. Hart, 1988), however similar sickness behaviours are also observed in insects (e.g., crickets). We predicted that immune-challenged crickets (Gryllus texensis) would reduce feeding, grooming, and locomotion as well as increase shelter use, consistent with the energy conservation and predator avoidance hypotheses. We found evidence of illness-induced anorexia in adult and juvenile crickets, consistent with previous research (Adamo et al., 2010), but contrary to expectations, we found an increase in grooming, and no evidence that crickets decreased locomotion or increased shelter use in response to immune challenge. Therefore, our results do not support the energy conservation or predator avoidance hypotheses. The difference in sickness behaviour between insects and mammals is probably due, in part, to the lack of physiological fever in insects. We hypothesize that the lack of physiological fever reduces the need for energy conservation, decreasing the benefits of some sickness behaviours such as increased shelter use. These results, taken together with others in the literature, suggest that ectotherms and endotherms may differ significantly in the selective forces leading to the evolution of most sickness behaviours.
Asunto(s)
Conducta Animal , Gryllidae , Conducta de Enfermedad , Animales , Evolución Biológica , Especificidad de la EspecieRESUMEN
Animals have a number of behavioral defenses against infection. For example, they typically avoid sick conspecifics, especially during mating. Most animals also alter their behavior after infection and thereby promote recovery (i.e., sickness behavior). For example, sick animals typically reduce the performance of energetically demanding behaviors, such as sexual behavior. Finally, some animals can increase their reproductive output when they face a life-threatening immune challenge (i.e., terminal reproductive investment). All of these behavioral responses probably rely on immune/neural communication signals for their initiation. Unfortunately, this communication channel is prone to manipulation by parasites. In the case of sexually transmitted infections (STIs), these parasites/pathogens must subvert some of these behavioral defenses for successful transmission. There is evidence that STIs suppress systemic signals of immune activation (e.g., pro-inflammatory cytokines). This manipulation is probably important for the suppression of sickness behavior and other behavioral defenses, as well as for the prevention of attack by the host's immune system. For example, the cricket, Gryllus texensis, is infected with an STI, the iridovirus IIV-6/CrIV. The virus attacks the immune system, which suffers a dramatic decline in its ability to make proteins important for immune function. This attack also hampers the ability of the immune system to activate sickness behavior. Infected crickets cannot express sickness behavior, even when challenged with heat-killed bacteria. Understanding how STIs suppress sickness behavior in humans and other animals will significantly advance the field of psychoneuroimmunology and could also provide practical benefits.
Asunto(s)
Afrodisíacos/farmacología , Conducta Animal , Interacciones Huésped-Parásitos/fisiología , Invertebrados/fisiología , Invertebrados/parasitología , Vertebrados/fisiología , Vertebrados/parasitología , AnimalesRESUMEN
Interactions between immune systems, nervous systems, and behavior are well established in vertebrates. A comparative examination of these interactions in other animals will help us understand their evolution and present adaptive functions. Insects show immune-behavioral interactions similar to those seen in vertebrates, suggesting that many of them may have a highly conserved function. Activation of an immune response in insects results in illness-induced anorexia, behavioral fever, changes in reproductive behavior, and decreased learning ability in a broad range of species. Flight-or-fight behaviors result in a decline in disease resistance. In insects, illness-induced anorexia may enhance immunity. Stress-induced immunosuppression is probably due to physiological conflicts between the immune response and those of other physiological processes. Because insects occupy a wide range of ecological niches, they will be useful in examining how some immune-behavioral interactions are sculpted by an animal's behavioral ecology.