Latitudinal variation of immune defense and sickness behavior in the white-crowned sparrow (Zonotrichia leucophrys).

There is a general trend that parasitism risk declines as latitude increases. Host populations breeding at high latitudes should therefore invest less in costly immune defenses than populations breeding in temperate or tropical zones, although it is unknown if such an effect is mediated by environmental (photoperiodic) or genetic factors or both. Acquired immune function (humoral, cell-mediated) and behavioral sickness responses to lipopolysaccharide (LPS; mimics bacterial infection) were assessed in two subspecies of white-crowned sparrow (Zonotrichia leucophrys) that breed at different latitudes in western North America. Zonotrichia l. gambelii (GWCS) is a high-latitude breeder (47-68 degrees N) while Z. l. pugetensis (PWCS) breeds at temperate latitudes (40-49 degrees N). Captive males of each subspecies were acclimated to (1) a short day (non-breeding) photoperiod (8L:16D), (2) the breeding photoperiod of PWCS (16L:8D), or (3) the breeding photoperiod of GWCS (20L:4D). Photoperiod was manipulated because shorter day lengths may enhance immune function. In support of a genetic effect, humoral responses to diphtheria-tetanus vaccination were significantly higher in PWCS compared to GWCS, regardless of photoperiod. There were no differences in cell-mediated responses to phytohemagglutinin (PHA) between subspecies or among photoperiods. For sickness responses to LPS, a significant interaction between photoperiod and subspecies was found, with long day GWCS producing stronger sickness responses (losing more weight, eating less) than short day GWCS and PWCS on all day lengths. However, these effects were influenced by photoperiodic changes in body condition. In conclusion, we find evidence for genetic control of immune responses across latitude, but no support for environmental (photoperiodic) regulation.

Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows.

The immunocompetence handicap hypothesis proposes that testosterone (T)-dependent sexual signals are honest indicators of male health or genetic quality because only high-quality males are able to withstand the obligate effects of T-induced immunosuppression. In birds, the basic assumption that T suppresses immune function is equivocal, and the physiological mechanisms underlying T-induced immunosuppression remain to be investigated. We explored the proximate pathways of T-induced immunosuppression in song sparrows (Melospiza melodia) by treating captive nonbreeding males with different androgens and measuring several components of acquired immune function. Males implanted with T suppressed cell-mediated and humoral immune responses compared to males implanted with 5alpha-dihydrotestosterone (DHT), dehydroepiandrosterone, or control (empty) implants. Furthermore, T treatment increased plasma levels of corticosterone and decreased body mass and fat stores in relation to other treatments. The failure of DHT to depress immune function suggests that T-induced immunosuppression does not occur through a direct pathway because both T and DHT bind to androgen receptors on target cells. Instead, we outline indirect pathways that are likely responsible for suppression of the avian immune system that include stress-induced immunosuppression, aromatization to estrogen, and alterations in energy allocation that constrain expenditures toward immune system activation.

Androgens, interspecific competition and species replacement in hybridizing warblers.

The steroid hormone testosterone regulates aggressive behaviour in many vertebrates and is important for territorial defence among males of the same species. However, its role in mediating interspecific competition, and ultimately species distributions, is unknown. We show that testosterone may influence the geographical replacement of one species by another. Townsend's warblers (Dendroica townsendi) have replaced hermit warblers (D. occidentalis) over a vast portion of their historical range, partly because Townsend's males are more aggressive than hermit males and outcompete them for territories in areas of sympatry. We report differences in plasma androgen levels that parallel these aggressive asymmetries and the historical pattern of species replacement between Townsend's and hermits. Using hybrids, we provide evidence that these hormonal differences are partially genetically based and thus may have evolved through sexual selection during Pleistocene glacial maxima. Hormone-behaviour mechanisms can therefore have important effects on species distributions and can even influence the pathways underlying extinction.

Modulation of the hypothalamic-pituitary-adrenal axis of an Arctic-breeding polygynandrous songbird, the Smith's longspur, Calcarius pictus.

To successfully reproduce in the Arctic, birds must modulate their neuroendocrine and behavioural systems. These adjustments include an attenuation of the stress responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis to external stimuli and a behavioural insensitivity to high corticosterone (B) levels. The HPA axis was examined in free-living territorial polygynandrous Smith's longspurs (Calcarius pictus) that migrate to breed on the Arctic tundra. Basal and stress-induced B levels were measured through the breeding season and were found to be significantly lower in females compared with males. This was not a consequence of adrenal insensitivity, because intrajugular injections of adrenocorticotrophin hormone (ACTH) enhanced B release in incubating females. In males the adrenocortical response to stress was significantly attenuated during the parental phase compared with arrival at the breeding ground. In contrast to temperate passerines, there was no significant decrease in male territorial aggressive behaviour when B was experimentally elevated, suggesting a behavioural insensitivity to glucocorticoids. This mechanism is hypothesized to increase reproductive success by preventing interruptions to parental care during transient deleterious environmental perturbations, which are often experienced in the short Arctic breeding season. Modulation of the HPA axis in this species in relation to life-history stage, lifetime reproductive success and the polygynandrous mating system is discussed.

Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna).

A variety of vertebrate species modulate immune function on a seasonal basis to cope with seasonal energy deficits and competing life-history demands, such as reproduction. Most studies to date have focused upon seasonal variation of cellular and humoral immunity, while neglecting behavioral responses to infection. These behavioral strategies are collectively termed sickness behaviors and are hypothesized to divert energy away from normal activities to combat and overcome infection. Sickness behavior can be triggered experimentally by injecting bacterial lipopolysaccharide (LPS). In this study, we provide the first evidence for seasonal modulation of sickness behavior in a free-living animal. Male song sparrows of western Washington state (Melospiza melodia morphna) are sedentary and territorial year round, except for a brief time during molt. Treatment with LPS decreased territorial aggressive behavior of males in the winter (nonbreeding), but not in the spring (breeding). Subjects were recaptured approx. 25 h after treatment. Recaptured LPS males in the winter lost more body mass than saline-injected controls while LPS males in the spring did not. These data indicate that birds in breeding condition were relatively insensitive to the effects of LPS. On a proximate level, suppression of sickness behavior during breeding is likely mediated by seasonal differences in energy allocation, as wintering sparrows were significantly heavier and had larger subcutaneous fat reserves and lower baseline corticosterone levels than breeding birds. Ultimately, suppression of sickness behavior may represent an allocation strategy to balance current reproductive opportunities with the life-history costs of self-defense.

Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii).

Exposing vertebrates to pathogenic organisms or inflammatory stimuli, such as bacterial lipopolysaccharide (LPS), activates the immune system and triggers the acute phase response. This response involves fever, alterations in neuroendocrine circuits, such as hypothalamo-pituitary-adrenal (HPA) and -gonadal (HPG) axes, and stereotypical sickness behaviors that include lethargy, anorexia, adipsia, and a disinterest in social activities. We investigated the hormonal, behavioral, and thermoregulatory effects of acute LPS treatment in a seasonally breeding songbird, the white-crowned sparrow (Zonotrichia leucophrys gambelii) using laboratory and field experiments. Captive male and female sparrows were housed on short (8L:16D) or long (20L:4D) day lengths and injected subcutaneously with LPS or saline (control). LPS treatment activated the HPA axis, causing a rapid increase in plasma corticosterone titers over 24 h compared to controls. Suppression of the HPG axis occurred in long-day LPS birds as measured by a decline in luteinizing hormone levels. Instead of a rise in body temperature, LPS-injected birds experienced short-term hypothermia compared to controls. Birds treated with LPS decreased activity and reduced food and water intake, resulting in weight loss. LPS males on long days experienced more weight loss than LPS males on short days, but this seasonal effect was not observed in females. These results paralleled seasonal differences in body condition, suggesting that modulation of the acute phase response is linked to energy reserves. In free-living males, LPS treatment decreased song and several measures of territorial aggression. These studies highlight immune-endocrine-behavior interrelationships that may proximately mediate life-history tradeoffs between reproduction and defense against pathogens.