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1.
J Exp Biol ; 220(Pt 5): 868-875, 2017 03 01.
Article in English | MEDLINE | ID: mdl-28011823

ABSTRACT

Although predator exposure increases the risk of wound infections, it typically induces immunosuppression. A number of non-mutually exclusive hypotheses have been put forward to explain this immunosuppression, including: trade-offs between the immune system and other systems required for anti-predator behaviour, redistribution of immune resources towards mechanisms needed to defend against wound infections, and reconfiguration of the immune system to optimize defence under the physiological state of fight-or-flight readiness. We tested the ability of each hypothesis to explain the effects of chronic predator stress on the immune system of the caterpillar Manduca sexta Predator exposure induced defensive behaviours, reduced mass gain, increased development time and increased the concentration of the stress neurohormone octopamine. It had no significant effect on haemocyte number, melanization rate, phenoloxidase activity, lysozyme-like activity or nodule production. Predator stress reduced haemolymph glutathione concentrations. It also increased constitutive expression of the antimicrobial peptide attacin-1 but reduced attacin-1 expression in response to an immune challenge. These results best fit the immune reconfiguration hypothesis, although the other hypotheses are also consistent with some results. Interpreting stress-related changes in immune function may require an examination at the level of the whole organism.


Subject(s)
Manduca/physiology , Predatory Behavior , Stress, Physiological , Animals , Escape Reaction , Gene Expression Regulation , Glutathione/analysis , Glutathione/immunology , Hemocytes/cytology , Hemocytes/immunology , Hemolymph/immunology , Immune Tolerance , Insect Proteins/analysis , Insect Proteins/immunology , Manduca/cytology , Manduca/genetics , Manduca/immunology , Octopamine/analysis , Octopamine/immunology
2.
J Exp Biol ; 219(Pt 23): 3750-3758, 2016 12 01.
Article in English | MEDLINE | ID: mdl-27634401

ABSTRACT

Some parasites alter the behaviour of their hosts. The larvae of the parasitic wasp Cotesia congregata develop within the body of the caterpillar Manduca sexta During the initial phase of wasp development, the host's behaviour remains unchanged. However, once the wasps begin to scrape their way out of the caterpillar, the caterpillar host stops feeding and moving spontaneously. We found that the caterpillar also temporarily lost sensation around the exit hole created by each emerging wasp. However, the caterpillars regained responsiveness to nociception in those areas within 1 day. The temporary reduction in skin sensitivity is probably important for wasp survival because it prevents the caterpillar from attacking the emerging wasp larvae with a defensive strike. We also found that expression of plasmatocyte spreading peptide (PSP) and spätzle genes increased in the fat body of the host during wasp emergence. This result supports the hypothesis that the exiting wasps induce a cytokine storm in their host. Injections of PSP suppressed feeding, suggesting that an augmented immune response may play a role in the suppression of host feeding. Injection of wasp larvae culture media into non-parasitized caterpillars reduced feeding, suggesting that substances secreted by the wasp larvae may help alter host behaviour.


Subject(s)
Behavior, Animal/physiology , Feeding Behavior/physiology , Larva/growth & development , Larva/metabolism , Manduca/physiology , Wasps/physiology , Animals , Intercellular Signaling Peptides and Proteins , Nociception/physiology , Peptides/genetics , Peptides/metabolism
3.
J Exp Biol ; 219(Pt 5): 706-18, 2016 Mar.
Article in English | MEDLINE | ID: mdl-26747906

ABSTRACT

Dwindling resources might be expected to induce a gradual decline in immune function. However, food limitation has complex and seemingly paradoxical effects on the immune system. Examining these changes from an immune system network perspective may help illuminate the purpose of these fluctuations. We found that food limitation lowered long-term (i.e. lipid) and short-term (i.e. sugars) energy stores in the caterpillar Manduca sexta. Food limitation also: altered immune gene expression, changed the activity of key immune enzymes, depressed the concentration of a major antioxidant (glutathione), reduced resistance to oxidative stress, reduced resistance to bacteria (Gram-positive and -negative bacteria) but appeared to have less effect on resistance to a fungus. These results provide evidence that food limitation led to a restructuring of the immune system network. In severely food-limited caterpillars, some immune functions were enhanced. As resources dwindled within the caterpillar, the immune response shifted its emphasis away from inducible immune defenses (i.e. those responses that are activated during an immune challenge) and increased emphasis on constitutive defenses (i.e. immune components that are produced consistently). We also found changes suggesting that the activation threshold for some immune responses (e.g. phenoloxidase) was lowered. Changes in the configuration of the immune system network will lead to different immunological strengths and vulnerabilities for the organism.


Subject(s)
Manduca/growth & development , Manduca/immunology , Animals , Bacillus cereus/immunology , Beauveria/immunology , Food Deprivation , Gene Expression Regulation, Developmental , Hemolymph/chemistry , Immune System/physiology , Larva/immunology , Larva/metabolism , Manduca/metabolism , Manduca/microbiology , Serratia marcescens/immunology
4.
J Exp Biol ; 217(Pt 11): 1970-6, 2014 Jun 01.
Article in English | MEDLINE | ID: mdl-24625650

ABSTRACT

We identified the insect iridovirus IIV-6/CrIV as a pathogen of the cricket Gryllus texensis using electron microscopy (EM) and polymerase chain reaction (PCR) analysis. EM showed that the virus attacks the fat body, an organ important for protein production, immune function and lipid storage. During infection the fat body hypertrophied, but egg production withered, leaving the lateral oviducts empty of eggs; the females were effectively sterile. EM of the testis of infected males suggests that the testis was not invaded by the virus, although sperm taken from the spermatophores of infected males showed little or no motility. Nevertheless, males and females continued to mate when infected. In fact, infected males were quicker to court females than uninfected controls. The virus benefits from the continued sexual behaviour of its host; transmission studies show that the virus can be spread through sexual contact. Sickness behaviour, the adaptive reduction of feeding and sexual behaviour that is induced by an activated immune system, was absent in infected crickets. Total haemolymph protein was reduced, as was phenoloxidase activity, suggesting a reduction in immune protein production by the fat body. The evidence suggests that during IIV-6/CrIV infection, the immune signal(s) that induces sickness behaviour is absent. Curtailment of a host's sickness behaviour may be necessary for any pathogen that is spread by host sexual behaviour.


Subject(s)
Aphrodisiacs , Copulation/physiology , Gryllidae/virology , Iridovirus/physiology , Ovary/virology , Spermatozoa/virology , Animals , Behavior, Animal , Fat Body/virology , Female , Immune System/pathology , Male , Sexually Transmitted Diseases, Viral
5.
J Exp Biol ; 216(Pt 24): 4608-14, 2013 Dec 15.
Article in English | MEDLINE | ID: mdl-24307711

ABSTRACT

Predator-induced stress responses are thought to reduce an animal's risk of being eaten. Therefore, these stress responses should enhance anti-predator behaviour. We found that individual insects (the cricket Gryllus texensis) show reliable behavioural responses (i.e. behavioural types) in a plus-shaped maze. An individual's behaviour in the plus maze remained consistent for at least 1/2 of its adult life. However, after exposure to a model predator, both male and female crickets showed a reduced period of immobility and an increased amount of time spent under shelter compared with controls. These changes could be mimicked by injections of the insect stress neurohormone octopamine. These behavioural changes probably aid crickets in evading predators. Exposure to a model predator increased the ability of crickets to escape a live predator (a bearded dragon, Pogona vitticeps). An injection of octopamine had the same effect, showing that stress hormones can reduce predation. Using crickets to study the fitness consequences of predator-induced stress responses will help integrate ecological and biomedical concepts of 'stress'.


Subject(s)
Escape Reaction , Gryllidae/physiology , Stress, Physiological , Animals , Female , Male , Octopamine/metabolism , Predatory Behavior , Reptiles/physiology
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