A direct physiological trade-off between personal and social immunity

1. Recent work shows that organisms possess two strategies of immune response: personal immunity, which defends an individual, and social immunity, which protects other individuals, such as kin. However, it is unclear how individuals divide their limited resources between protecting themselves and protecting others.
2. Here, with experiments on female burying beetles, we challenged the personal immune system and measured subsequent investment in social immunity (antibacterial activity of the anal exudates).
3. Our results show that increased investment in one aspect of personal immunity (wound repair) causes a temporary decrease in one aspect of the social immune response.
4. Our experiments further show that by balancing investment in personal and social immunity in this way during one breeding attempt, females are able to defend their subsequent lifetime reproductive success.
5. We discuss the nature of the physiological trade-off between personal and social immunity in species that differ in the degree of eusociality and coloniality, and suggest that it may also vary within species in relation to age and partner contributions to social immunity.

Parental care influences social immunity in burying beetle larvae

In this study, evidence is provided of social immunity in the offspring of a sub-social species, the burying beetle, Nicrophorus vespilloides. Nicrophorus vespilloides is a carrion breeder and, in a similar fashion to the adult beetles, the offspring produce exudates that exhibit lytic activity, which are used to coat the breeding resource. This strategy defends against the microbial community. The lytic activity in larval exudates declines as the brood develops, perhaps being most beneficial at the start of the breeding bout. Changing levels of parental care through widowing/orphaning affects lytic activity in the larval exudates, with levels decreasing in the absence of both parents.

Trade-offs between personal immunity and reproduction in the burying beetle, Nicrophorus vespilloides

How are resources split between caring for offspring and self-maintenance? Is the timing of immune challenge important? In burying beetles challenging the immune system prior to breeding does not affect the total number and quality of offspring produced during the individual's lifetime. However, the immune system is suppressed during breeding and if an immune challenge is presented during this time the beetle will upregulate its immune system, but at the detriment to the number of offspring produced during that breeding opportunity.We know that parental investment and immune investment are costly processes, but it is unclear which trait will be prioritized when both may be required. Here, we address this question using the burying beetle Nicrophorus vespilloides, carrion breeders that exhibit biparental care of young. Our results show that immunosuppression occurs during provision of parental care. We measured phenoloxidase (PO) on Days 1-8 of the breeding bout and results show a clear decrease in PO immediately from presentation of the breeding resource onward. Having established baseline immune investment during breeding we then manipulated immune investment at different times by applying a wounding challenge. Beetles were wounded prior to and during the parental care period and reproductive investment quantified. Different effects on reproductive output occur depending on the timing of wounding. Challenging the immune system with wounding prior to breeding does not affect reproductive output and subsequent lifetime reproductive success (LRS). LRS is also unaffected by applying an immune elicitor prior to breeding, though different arms of the immune system are up/downregulated, perhaps indicating a trade-off between cellular and humoral immunity. In contrast, wounding during breeding reduces reproductive output and to the greatest extent if the challenge is applied early in the breeding bout. Despite being immunosuppressed, breeding beetles can still respond to wounding by increasing PO, albeit not to prebreeding levels. This upregulation of PO during breeding may affect parental investment, resulting in a reduction in reproductive output. The potential role of juvenile hormone in controlling this trade-off is discussed.

Aging in personal and social immunity: do immune traits senesce at the same rate?

How much should an individual invest in immunity as it grows older? Immunity is costly and its value is likely to change across an organism's lifespan. A limited number of studies have focused on how personal immune investment changes with age in insects, but we do not know how social immunity, immune responses that protect kin, changes across lifespan, or how resources are divided between these two arms of the immune response. In this study, both personal and social immune functions are considered in the burying beetle, Nicrophorus vespilloides. We show that personal immune function declines (phenoloxidase levels) or is maintained (defensin expression) across lifespan in nonbreeding beetles but is maintained (phenoloxidase levels) or even upregulated (defensin expression) in breeding individuals. In contrast, social immunity increases in breeding burying beetles up to middle age, before decreasing in old age. Social immunity is not affected by a wounding challenge across lifespan, whereas personal immunity, through PO, is upregulated following wounding to a similar extent across lifespan. Personal immune function may be prioritized in younger individuals in order to ensure survival until reproductive maturity. If not breeding, this may then drop off in later life as state declines. As burying beetles are ephemeral breeders, breeding opportunities in later life may be rare. When allowed to breed, beetles may therefore invest heavily in "staying alive" in order to complete what could potentially be their final reproductive opportunity. As parental care is important for the survival and growth of offspring in this genus, staying alive to provide care behaviors will clearly have fitness payoffs. This study shows that all immune traits do not senesce at the same rate. In fact, the patterns observed depend upon the immune traits measured and the breeding status of the individual.

Antimicrobial capacity of plasma from anurans of the Atlantic Forest

The viability and interpretation of techniques for the evaluation of immunocompetence of animals in their natural environment has been largely debated. One of these methods is based on testing the antimicrobial capacity of the blood and/or plasma in vitro, which could rapidly and effectively assess the immunological conditions of natural populations. We tested the applicability of the antimicrobial capacity of plasma (ACP) assay in anuran amphibians from the Atlantic Forest. The assay was performed by measuring both the turbidity (in a spectrophotometer) and the colony forming units (CFU) of the remaining bacteria (Escherichia coli) following exposure to amphibian plasma. Although both assays were correlated, the ACP assay by spectrophotometry showed 10 times lower intra-assay variation. We also found interspecific variation in ACP, as well as the maintenance of ACP values in males from the same population, collected in different breeding seasons. Thus, the estimation of ACP by spectrophotometry provides a convenient and accurate method for evaluating innate immunocompetence in comparative and ecophysiological studies of anuran amphibians.

Personality and innate immune defenses in a wild bird: evidence for the pace-of-life hypothesis

We tested the two main evolutionary hypotheses for an association between immunity and personality. The risk-of-parasitism hypothesis predicts that more proactive (bold, exploratory, risk-taking) individuals have more vigorous immune defenses because of increased risk of parasite exposure. In contrast, the pace-of-life hypothesis argues that proactive behavioral styles are associated with shorter lifespans and reduced investment in immune function. Mechanistically, associations between immunity and personality can arise because personality differences are often associated with differences in condition and stress responsiveness, both of which are intricately linked with immunity. Here we investigate the association between personality (measured as proactive exploration of a novel environment) and three indices of innate immune function (the non-specific first line of defense against parasites) in wild superb fairy-wrens Malurus cyaneus. We also quantified body condition, hemoparasites (none detected), chronic stress (heterophil:lymphocyte ratio) and circulating corticosterone levels at the end of the behavioral test (CORT, in a subset of birds). We found that fast explorers had lower titers of natural antibodies. This result is consistent with the pace-of-life hypothesis, and with the previously documented higher mortality of fast explorers in this species. There was no interactive effect of exploration score and duration in captivity on immune indices. This suggests that personality-related differences in stress responsiveness did not underlie differences in immunity, even though behavioral style did modulate the effect of captivity on CORT. Taken together these results suggest reduced constitutive investment in innate immune function in more proactive individuals.

Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus

The microsporidian parasite, Pleistophora mulleri, infects the abdominal muscle of the freshwater amphipod Gammarus duebeni celticus. We recently showed that P. mulleri infection was associated with G. d. celticus hosts being more vulnerable to predation by the invasive amphipod Gammarus pulex. Parasitized G. d. celticus also had a reduced ability to prey upon other co-occurring amphipods. We suggested the parasite may have pervasive influences on host ecology and behaviour. Here, we examine the association between P. mulleri parasitism and parameters influencing individual host fitness, behaviour and interspecific interactions. We also investigate the relationship between parasite prevalence and host population structure in the field. In our G. d. celticus study population, P. mulleri prevalence was strongly seasonal, ranging from 8.5% in summer to 44.9% in winter. The relative abundance of hosts with the heaviest parasite burden increased during summer, which coincided with high host mortality, suggesting that parasitism may regulate host abundance to some degree. Females were more likely to be parasitized than males and parasitized males were paired with smaller females than unparasitized males. Parasitism was associated with reduction in the host's activity level and reduced both its predation on the isopod Asellus aquaticus and aggression towards precopula pairs of the invasive G. pulex. We discuss the pervasive influence of this parasite on the ecology of its host.

Integrating nutrition and immunology: A new frontier

Nutrition is critical to immune defence and parasite resistance, which not only affects individual organisms, but also has profound ecological and evolutionary consequences. Nutrition and immunity are complex traits that interact via multiple direct and indirect pathways, including the direct effects of nutrition on host immunity but also indirect effects mediated by the host's microbiota and pathogen populations. The challenge remains, however, to capture the complexity of the network of interactions that defines nutritional immunology. The aim of this paper is to discuss the recent findings in nutritional research in the context of immunological studies. By taking examples from the entomological literature, we argue that insects provide a powerful tool for examining the network of interactions between nutrition and immunity due to their tractability, short lifespan and ethical considerations. We describe the relationships between dietary composition, immunity, disease and microbiota in insects, and highlight the importance of adopting an integrative and multi-dimensional approach to nutritional immunology. 

Review article : ecological approach in studying the relation of perception-action : review of the theoretical and empirical data

In daily activities people are using a number of available means for the achievement of balance, such as the use of hands and the co-ordination of balance. One of the approaches that explains this relationship between perception and action is the ecological theory that is based on the work of a) Bernstein (1967), who imposed the problem of ‘the degrees of freedom’, b) Gibson (1979), who referred to the theory of perception and the way which the information is received from the environment in order for a certain movement to be achieved, c) Newell (1986), who proposed that movement can derive from the interaction of the constraints that imposed from the environment and the organism and d) Kugler, Kelso and Turvey (1982), who showed the way which “the degrees of freedom” are connected and interact. According to the above mentioned theories, the development of movement co-ordination can result from the different constraints that imposed into the organism-environment system. The close relation between the environmental and organismic constraints, as well as their interaction is responsible for the movement system that will be activated. These constraints apart from shaping the co-ordination of specific movements can be a rate limiting factor, to a certain degree, in the acquisition and mastering of a new skill. This frame of work can be an essential tool for the study of catching an object (e.g., a ball). The importance of this study becomes obvious due to the fact that movements that involved in catching an object are representative of every day actions and characteristic of the interaction between perception and action.

Information–movement coupling in developing cricketers under changing ecological practice constraints

Changing informational constraints of practice, such as when using ball projection machines, has been shown to significantly affect movement coordination of skilled cricketers. To date, there has been no similar research on movement responses of developing batters, an important issue since ball projection machines are used heavily in cricket development programmes. Timing and coordination of young cricketers (n = 12, age = 15.6 ± 0.7 years) were analyzed during the forward defensive and forward drive strokes when facing a bowling machine and bowler (both with a delivery velocity of 28.14 ± 0.56 m s−1). Significant group performance differences were observed between the practice task constraints, with earlier initiation of the backswing, front foot movement, downswing, and front foot placement when facing the bowler compared to the bowling machine. Peak height of the backswing was higher when facing the bowler, along with a significantly larger step length. Altering the informational constraints of practice caused major changes to the information–movement couplings of developing cricketers. Data from this study were interpreted to emanate from differences in available specifying variables under the distinct practice task constraints. Considered with previous findings, results confirmed the need to ensure representative batting task constraints in practice, cautioning against an over-reliance on ball projection machines in cricket development programmes.

Ecological approaches to cognition and action in sport and exercise : ask not only what you do, but where you do it

In recent decades, concepts and ideas from James J. Gibson’s theory of direct perception in ecological psychology have been applied to the study of how perception and action regulate sport performance. This article examines the influence of different streams of thought in ecological psychology for studying cognition and action in the diverse behavioural contexts of sport and exercise. In discussing the origins of ecological psychology it can be concluded that psychologists such as Lewin, and to some extent Heider, provided the initial impetus for the development of key ideas. We argue that the papers in this special issue clarify that the different schools of thinking in ecological psychology have much to contribute to theoretical and practical developments in sport and exercise psychology. For example, Gibson emphasized and formalized how the individual is coupled with the environment; Brunswik raised the issue of the ontology of probability in human behaviour and the problem of representative design for experimental task constraints; Barker looked carefully into extra-individual behavioural contexts and Bronfenbrenner presented insights pertinent to the relations between behaviour contexts, and macro influences on behaviour. In this overview, we highlight essential issues from the main schools of thought of relevance to the contexts of sport and exercise, and we consider some potential theoretical linkages with dynamical systems theory.

The development of decision making skill in sport : An ecological dynamics perspective

In this chapter we introduce a theoretical framework for studying decision making in sport: the ecological dynamics approach, which we integrate with key ideas from the literature on learning complex motor skills. Our analysis will include insights from Berstein (1967) on the coordination of degrees of freedom and Newell's (1985) model of motor learning. We particularly focus on the role of perceptual degrees of freedom advocated in an ecological approach to learning. In introducing this framework to readers we contrast this perspective with more traditional models of decision-making. Finally, we propose some implications to the training of decision-making skill in sport.