Trade-offs between behavioural traits promoting high life-history productivity and mortality may fuel the evolution of animal personalities. We propose that parasites, including pathogens, impose fitness costs comparable to those from predators, and influence the adaptiveness of personality traits associated with productivity (PAPs). Whether personality traits are adaptive or not may also depend on individual immunological capacity. We illustrate this using a conceptual example in which the optimal level of PAPs depends on predation, parasitism and host compensation (resistance and tolerance) of parasitism's negative effects. We assert that inherent differences in host immune function can produce positive feedback loops between resource intake and compensation of parasitism's costs, thereby providing variation underlying the evolution of stable personalities. Our approach acknowledges the condition dependence of immune function and co-evolutionary dynamics between hosts and parasites.
The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of mate quality because the hormones (e.g. testosterone) needed to develop secondary sexual traits have immunosuppressive effects. The best support for predictions arising from the immunocompetence handicap hypothesis so far comes from studies of insects, although they lack male-specific hormones such as testosterone. In our previous studies, we found that female mealworm beetles prefer pheromones of immunocompetent males. Here, we tested how juvenile hormone ( JH) affects male investment in secondary sexual characteristics and immune functions in the mealworm beetle, Tenebrio molitor. We injected male mealworm beetles with JH (type III) and found that injection increased the attractiveness of male pheromones but simultaneously suppressed immune functions (phenoloxidase activity and encapsulation). Our results suggest that JH, which is involved in the control of reproduction and morphogenesis, also plays a central role in the regulation of a trade-off between the immune system and sexual advertisement in insects. Thus, the results reflect a general mechanism by which the immunocompetence handicap hypothesis may work in insects.
Pheromones function not only as mate attractors, but they may also relay important information to prospective mates. It has been shown that vertebrates can distinguish, via olfactory mechanisms, major histocompatibility complex types in their prospective mates. However, whether pheromones can transmit information about immunocompetence is unknown. Here, we show that female mealworm beetles (Tenebrio molitor) prefer pheromones from males with better immunocompetence, indicated by a faster encapsulation rate against a novel antigen, and higher levels of phenoloxidase in haemolymph. Thus, the present study indicates that pheromones could transmit information about males' parasite resistance ability and may work as a reliable sexual ornament for female choice.
Summary 1.Pheromones are chemical signals that function not only as mate attractors, but may also relay important information to prospective mates. In order for the information to be reliable, the signal must be costly to produce and this is likely to result in condition dependent expression of the signal. 2. We present results from two experiments on the grain beetle Tenebrio molitor examining phenotypic condition dependence of pheromones and patterns of female preference for pheromones. We also analysed condition dependence of two measures of immunocompetence: encapsulation response and phenoloxidase activity. 3. By manipulating the nutritional condition of the males we found that the attractiveness of the male pheromones to virgin females was condition-dependent, indicating that the production of the pheromones is affected by the condition of the male. We also found that the phenoloxidase activity of the males was affected by the nutritional condition of the male but that encapsulation rate was not. 4. Our results show that pheromones are condition-dependent signals, the quantity of which females use in their mate choice.
It has been assumed that sexual ornaments have evolved to reveal males’ health and vigour for females. Choosy females may indirectly use ornaments as an indicator of the presence and effectiveness of genes for resistance against parasites. In this study we tested whether females of the Mediterranean field cricket, Gryllus bimaculatus, can use courtship song as a cue for choosing males with high immunocompetence, measured as encapsulation rate of nylon implants and lytic activity of haemolymph. We found that female crickets preferred courtship songs from males with a high encapsulation rate. Female crickets also had a tendency to prefer courtship songs with high tick rate and long high‐frequency tick duration. These preferred song components were positively correlated with encapsulation rate, but negatively correlated with lytic activity of the male. In contrast to previous studies of crickets, there was no correlation between male weight and encapsulation rate or lytic activity. There is some evidence in another cricket species that the ability to encapsulate pathogens is heritable. Thus, in light of this study it seems possible that by preferring males according to their courtship song, females might benefit by increasing the parasite resistance of their offspring. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 79, 503–510.
Summary1. According to a recent hypothesis, personality traits should form integrative pace-of-life syndromes with life-history traits. Potential life-history traits that explain personality variation are immune defence and growth rate. 2. We studied whether boldness, measured as hiding behaviour, is repeatable during ontogeny in the field cricket, Gryllus integer, and if it relates to the efficiency of immune function (i.e. the capacity to encapsulate a nylon implant), growth rate, developmental time and size as an adult. 3. Hiding behaviour was rank-order repeatable, and in general, juveniles were bolder than adults. Individuals that were cautious at early juvenile stages had higher encapsulation responses late in life compared with bold individuals. Most clearly, fast-growing individuals matured early and invested little in immune defence compared with their slower-growing conspecifics, i.e. showed patterns of a 'grow fast, die young' life-history strategy. 4. Our results may arise from a trade-off between immunity-dependent survival and bold behaviour. Trade-offs between investment in survival and behaviour could account for the maintenance of variation in personality traits by favouring certain combinations of behavioural and life-history strategies (i.e. pace-of-life-syndromes).
Seasonal changes in immunocompetence are predicted by the hypothesized trade‐off between reproduction and self‐maintenance, whereby immune function is a measure of self‐maintenance and reproductive effort is seasonally dependent. We examined seasonal patterns in immunological, haematological and body condition parameters for male and female freshwater fish. In two different populations, the relative size of the spleen and the chemotaxic migration activity of head kidney granulocytes decreased immediately before and after spawning, respectively. Those decreases were accompanied by an increase in haematocrit values shortly before and after spawning in both populations and a decrease in the relative body weight in one population, possibly due to physiological stress caused by increased activity during the spawning period. Breeding‐related changes in other measures studied (phagocytosis activity of head kidney granulocytes, blood IgM concentration, white cell count and red cell count) were absent or inconsistent. Some of the results are in line with the idea of a trade‐off between reproduction and immune defence. The present data suggest that the differential responses of the immune system may have different temporal patterns, which should be taken into account in immunoecological studies. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 117−127.
Behavioural syndromes, or suites of correlated behaviours across different contexts and situations, have recently drawn attention from evolutionary biologists. In the field cricket Gryllus integer , males are aggressive with one another and fight vigorously over females and territories. We examined whether aggressiveness with other males was correlated with activity in a potentially dangerous context (a novel environment) in laboratory-raised virgin males. Aggressiveness was measured as fighting ability against a weight-matched opponent. First, we measured each cricket's latency to become active in a novel environment and latency to emerge from a refuge within a novel environment. Next, we determined which of two weight-matched males was more aggressive, by pitting the males together in an agonistic contest and counting the number of fights won by each male. More aggressive males, who won more fights, had shorter latencies to become active when placed in a novel environment and shorter latencies to emerge from a safe refuge. These results suggest that a behavioural syndrome exists in G. integer , in which more aggressive males are also more active in general, and possibly less cautious towards predation risk.
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