Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

Abstract

Animals living in temporally dynamic environments experience variation in resource availability, climate and threat of infection over the course of the year. Thus, to survive and reproduce successfully, these organisms must allocate resources among competing physiological systems in such a way as to maximize fitness in changing environments. Here, we review evidence supporting the hypothesis that physiological trade-offs, particularly those between the reproductive and immune systems, mediate part of the seasonal changes detected in the immune defences of many vertebrates. Abundant recent work has detected significant energetic and nutritional costs of immune defence. Sometimes these physiological costs are sufficiently large to affect fitness (e.g. reproductive output, growth or survival), indicating that selection for appropriate allocation strategies probably occurred in the past. Because hormones often orchestrate allocations among physiological systems, the endocrine mediators of seasonal changes in immune activity are discussed. Many hormones, including melatonin, glucocorticoids and androgens have extensive and consistent effects on the immune system, and they change in systematic fashions over the year. Finally, a modified framework within which to conduct future studies in ecological immunology is proposed, viz. a heightened appreciation of the complex but intelligible nature of the vertebrate immune system. Although other factors besides trade-offs undoubtedly influence seasonal variation in immune defence in animals, a growing literature supports a role for physiological trade-offs and the fitness consequences they sometimes produce.

Figure 1

Comparisons of the (a) winter immunoenhancement versus the (b) trade-off models to explain seasonal variation in immune activity. According to the winter immunoenhancement model (a), immune activity is suppressed during winter (short days for most non-tropical seasonal breeders) due to the stressors of winter conditions (downward-pointing arrow), such as low ambient temperatures and food availability. This stress-induced immunosuppression is buffered by animals (upward-pointing arrow) in winter (short-day conditions in the laboratory) by increasing immune responses to levels greater than those that occur in long days. According to the trade-off model (b), immune activity is depressed when other costly physiological activities are concurrent, such as breeding (downward-pointing arrow). The schematic here depicts resource-driven immunosuppression during breeding, but this result would presumably hold for any other costly physiological process, such as tissue regeneration and growth, or perhaps even expensive behaviours (e.g. territory defence).

Figure 2

The immune defence component model (IDCM). This conceptualization of the immune system, originally proposed by Schmid-Hempel & Ebert (2003) separates immune defences into four quadrants representing the four types of defences available to animals. One axis represents a continuum from non-specific to specific defences, whereas the other axis represents static (constitutive) versus dynamic (induced) defences. In the figure, we categorize several of the assays currently favoured in ecological immunology (see table 1 for details of each assay). Adapted from Schmid-Hempel & Ebert (2003).