Does the strength of an immune response reflect its energetic cost?

SUMMARYAllocation trade-offs of limited resources are thought to ensure the honesty of sexual signals and are often studied using controlled immune challenges. One such trade-off between immunity and ornaments is that involving carotenoids. Phytohemagglutinin (PHA)-induced immune response is a widely used immune challenge, yet more details on the underlying physiological mechanisms and potential costs are needed. We investigated the temporal dynamics of PHA-induced immune response and associated changes in blood carotenoids, body mass and a carotenoid-based coloured signal. We found variation in individual response patterns to PHA after peak swelling was reached, with birds showing either a rapid or a slow subsequent decrease in swelling, suggesting variation in the duration of the immune response and/or inflammation. Body mass did not affect immune response. Plasma carotenoids followed a transient decrease closely matching the dynamics of the swelling. The peak of the immune response was negatively related to initial plasma carotenoid levels and positively correlated to the relative decrease in plasma carotenoids. Individual variation in duration of the swelling could be partly explained by plasma carotenoids; high initial carotenoid levels were associated with a slower decrease of the swelling. These contradictory effects of carotenoids suggest a complex role in the immune response. Bill colour was positively correlated to initial plasma carotenoid concentration but it did not predict or change as a consequence of immune response to PHA. Bill colour thus reflects medium-or long-term quality rather than immediate quality. Taking into account the dynamics of the immune response and that of associated physiological parameters would thus yield new insights into our interpretation of variation in PHA response.

Section: Discussionmentioning

confidence: 99%

Dynamics of PHA-induced immune response and plasma carotenoids in birds:should we have a closer look?

Biard

Hardy

Motreuil

et al. 2009

“…As such, they argued that such an energetic increase would be sufficient to influence an important life-history trait. By contrast, great tits (Parus major) injected with higher doses of PHA had stronger immune responses; however, an individual's metabolic rate (MR) was not dose-dependent, and was relatively low (Nilsson et al, 2007).…”

Section: Introductionmentioning

confidence: 97%

Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches?

Burness

Armstrong

Fee

et al. 2010

SUMMARYThere has been recent interest in understanding trade-offs between immune function and other fitness-related traits. At proximate levels, such trade-offs are presumed to result from the differential allocation of limited energy resources. Whether the costs of immunity are sufficient to necessitate such energy reallocation remains unclear. We tested the metabolic and behavioural response of male zebra finches (Taeniopygia guttata) to the combined effects of thermoregulation and generation of an acute phase response (APR). The APR is the first line of defence against pathogens, and is considered energetically costly. We predicted that at cold temperatures zebra finches would exhibit an attenuated APR when compared with individuals at thermoneutrality. We challenged individuals with bacterial lipopolysaccharide (LPS), an immunogenic compound that stimulates an APR. Following LPS injection, we measured changes in food intake, body mass, activity, and resting and total energy expenditure. When challenged with LPS under ad libitum food, individuals at both temperatures decreased food intake and activity, resulting in similar mass loss. In contrast to predicted energetic trade-offs, cold-exposed individuals injected with LPS increased their nocturnal resting energy expenditure more than did individuals held at thermoneutrality, yet paradoxically lost less mass overnight. Although responding to LPS was energetically costly, resulting in a 10% increase in resting expenditure and 16% increase in total expenditure, there were few obvious energetic trade-offs. Our data support recent suggestions that the energetic cost of an immune response may not be the primary mechanism driving trade-offs between immune system function and other fitness-related traits.

“…Ots et al, 2001;Freitak et al, 2003;Martin et al, 2003;Demas, 2004;Derting and Virk, 2005;Martin et al, 2008) (but see Nilsson et al, 2007). In addition, the costs associated with physiological (somatic) maintenance are often observed through phenotypic trade-offs with reproduction or performance (e.g.…”

Section: Introductionmentioning

confidence: 99%

State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta)

Schwanz

Warner

McGaugh

et al. 2011

SUMMARYEnergy allocation among somatic maintenance, reproduction and growth varies not only among species, but among individuals according to states such as age, sex and season. Little research has been conducted on the somatic (physiological) maintenance of long-lived organisms, particularly ectotherms such as reptiles. In this study, we examined sex differences and age-and seasonrelated variation in immune function and DNA repair efficiency in a long-lived reptile, the painted turtle (Chrysemys picta). Immune components tended to be depressed during hibernation, in winter, compared with autumn or spring. Increased heterophil count during hibernation provided the only support for winter immunoenhancement. In juvenile and adult turtles, we found little evidence for senescence in physiological maintenance, consistent with predictions for long-lived organisms. Among immune components, swelling in response to phytohemagglutinin (PHA) and control injection increased with age, whereas basophil count decreased with age. Hatchling turtles had reduced basophil counts and natural antibodies, indicative of an immature immune system, but demonstrated higher DNA repair efficiency than older turtles. Reproductively mature turtles had reduced lymphocytes compared with juvenile turtles in the spring, presumably driven by a trade-off between maintenance and reproduction. Sex had little influence on physiological maintenance. These results suggest that components of physiological maintenance are modulated differentially according to individual state and highlight the need for more research on the multiple components of physiological maintenance in animals of variable states. Supplementary material available online at