Energetic reserves, leptin and testosterone: a refinement of the immunocompetence handicap hypothesis

The immunocompetence handicap hypothesis (ICHH) assumes that testosterone (T), required for the expression of sexual traits, can also incur a cost due to its immunosuppressive properties. However, T-dependent immunosuppression could also arise as an indirect consequence of energy reallocation from the immune system to other metabolic demands. Leptin is mostly produced in lipogenic tissues and its circulating level is positively correlated with the amount of lipid reserves. Leptin also has an important role as immunoenhancer and we suggest that this hormone could play a role as a mediator of the immunosuppressive effect of testosterone. In particular, we propose that only the individuals able to maintain large lipid reserves (with high leptin levels), while sustaining high testosterone levels, might be able to develop sexual displays without an impairment of their immune defences. Here, we tested one of the assumptions underlying this extension of the ICHH: leptin administration should attenuate testosterone-induced immunosuppression. T-implanted and control male zebra finches (Taeniopygia guttata) received daily injections of leptin or phosphate buffered saline. T-implants initially depressed the phytohaemagglutinin-induced immune response. However, T-birds injected with leptin enhanced their immune response to the level of control birds. These results open a new perspective on the study of the ICHH.     

Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in Red Bishops Euplectes orix

The immunocompetence handicap hypothesis (ICHH) posits that the hormone testosterone mediates a trade‐off between investment in reproduction and immunological condition. In this study, we tested the ICHH in the Red Bishop Euplectes orix, a polygynous weaverbird. Males of this strongly sexually dimorphic species show an elaborate courtship display to attract females and compete aggressively with other males for nesting sites in breeding colonies. We experimentally elevated testosterone levels in breeding male Red Bishops kept in an aviary with a subcutaneous implantation of testosterone‐releasing pellets. We then compared behaviour, development of territory size and immunological condition (as assessed through a white blood cell count) of the experimental group with a control group treated with placebos. In addition, we measured the primary and secondary response to phytohaemagglutinin (PHA) to investigate the effect of testosterone on both innate and acquired immunity. Males with elevated levels of testosterone enlarged their territories and conducted more courtship behaviour, while showing a decrease in health, expressed by an increased heterophil/lymphocyte ratio compared with the control group. Males of the control group showed an increase of the secondary response to PHA, as expected under the assumption that repeated exposure to an antigen enhanced the immune response due to acquired immunity. However, males with experimentally increased testosterone levels did not show such an enhanced immune response in the secondary PHA test (although sample size and power of the statistical tests were low), indicating that testosterone treatment might directly or indirectly suppress some component of the acquired immune response.     

Energy metabolism, testosterone and corticosterone in white-crowned sparrows

The influence of the steroid hormones testosterone and corticosterone on energy metabolism and activity of birds is largely enigmatic. We measured resting metabolic rate during night and day in 12 long-term castrated and 12 intact male white-crowned sparrows (Zonotrichia leucophrys gambelii) under short-day (8:16 SD), long-day (20:4 LD), LD+testosterone implant and LD−testosterone implant conditions. Each male was sequentially measured under all four conditions. Photostimulation increased testosterone, resting metabolic rate, food intake, hopping activity and body mass in castrates and intact males. Surprisingly, testosterone levels and metabolic rates did not differ between intact and castrated males. Testosterone implantation increased activity and food intake, but decreased body mass and resting metabolic rate in both groups. Removing testosterone implants reversed the effects on resting metabolic rate, activity and food intake. Corticosterone levels, measured immediately at the end of metabolism measurements, showed birds were not stressed. Corticosterone had no apparent relationship with resting metabolic rate and there was no interaction between corticosterone and testosterone. Overall, positive changes in testosterone levels resulted in a decrease of resting metabolic rate. We speculate that testosterone increases activity, and birds compensate for increased activity metabolism by reducing resting metabolic rate. Accepted: 18 July 1999     

Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male garter snake, Thamnophis sirtalis

Stress and reproduction are generally thought to work in opposition to one another. This is often manifested as reciprocal relationships between glucocorticoid stress hormones and sex steroid hormones. However, seasonal differences in how animals respond to stressors have been described in extreme environments. We tested the hypothesis that garter snakes, Thamnophis sirtalis, with limited reproductive opportunities will suppress their hormonal stress response during the breeding season relative to conspecifics with an extended breeding season. The red-sided garter snake, T.s. parietalis, of Manitoba, Canada, has a brief breeding season during which males displayed no change in either plasma levels of testosterone or corticosterone, which were both elevated above basal levels, in response to capture stress. During the summer, capture stress resulted in increased plasma corticosterone and decreased testosterone. During the fall, when mating can also occur, males exhibited a significant decrease in testosterone but no increase in corticosterone in response to capture stress. The red-spotted garter snake, T.s. concinnus, of western Oregon, has an extended breeding season during which males displayed a stress response of increased plasma corticosterone and decreased testosterone levels. The corticosterone response to capture stress was similar during the spring, summer, and fall. In contrast, the testosterone response was suppressed during the summer and fall when gametogenesis was occurring. These data suggest that male garter snakes, in both populations, seasonally adapt their stress response but for different reasons and by potentially different mechanisms. J. Exp. Zool. 289:99-108, 2001.     

Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis

Species with alternative phenotypes offer unique opportunities to investigate hormone-behavior relationships. We investigated the relationships between testosterone, corticosterone, morphology, performance, and immunity in a population of lizards (Podarcis melisellensis) which exhibits a color polymorphism. Males occur in three different color morphs (white, yellow, orange), providing an opportunity to test the idea of morphs being alternative solutions to the evolutionary challenges posed on the link between hormones, morphology, performance, and immunity. Morphs differed in bite force capacity, with orange males biting harder, and in corticosterone levels, with yellow males having lower levels than orange. However, morphs did not differ in testosterone levels or in the immunological parameters tested. At the individual level, across morphs, testosterone levels predicted size-corrected bite force capacity, but no relation was found between hormone levels and immunity. Our results do not support the testosterone-based polymorphism hypothesis and reject the hypothesis of a trade-off between testosterone and immunity in this species, but provide a mechanistic link between testosterone and a sexually selected performance trait.     

Stress, social behaviour, and secondary sexual traits in a male primate

We examined variation in glucocorticoid levels in the mandrill, a brightly coloured primate species, to identify major social influences on stress hormones, and investigate relationships among glucocorticoid levels, testosterone and secondary sexual ornamentation. We collected a total of 317 fecal samples for 16 adult male mandrills over 13 months, including mating and non-mating periods and periods of both dominance rank stability and instability, and compared fecal glucocorticoid levels with dominance rank, rank stability, presence of receptive females, gastro-intestinal parasite infection, fecal testosterone and facial red coloration. Glucocorticoid levels did not vary systematically with dominance rank, but increased when the dominance hierarchy was unstable, and increased in the presence of receptive females. The relationship between dominance rank and glucocorticoid levels changed direction according to the stability of the dominance hierarchy: glucocorticoid levels were higher in subordinate males under stable conditions, but under conditions of instability higher ranking males had higher glucocorticoid levels. The influence of dominance rank also interacted with the presence of receptive females: glucocorticoids were higher in dominant males than in subordinates, but only during mating periods, suggesting that dominant males are more stressed than subordinates during such periods. These findings support previous studies showing that the relationship between glucocorticoids and dominance rank in male baboons is dependent on the social environment. We also found that males with higher glucocorticoids suffered a higher diversity of gastrointestinal parasite infection, in line with evidence that glucocorticoids suppress the immune system in other species. However, we found no support for the stress-mediated immunocompetence handicap hypothesis for the evolution of condition-dependent ornaments: glucocorticoid and testosterone levels were positively related, rather than the negative relationship predicted by the hypothesis, and we found no relationship between red colour and glucocorticoid levels, suggesting that glucocorticoids do not play a role in translating social conditions or physical health into ornament expression in this species.     

SUPPORT FOR THE IMMUNOCOMPETENCE HANDICAP HYPOTHESIS IN THE WILD: HORMONAL MANIPULATION DECREASES SURVIVAL IN SICK DAMSELFLIES

The immunocompetence handicap hypothesis (ICHH) states that hormones enhance sexual trait expression but impair immunity. Previous tests of the ICHH have been hampered by experimental design problems. Here, we report on an experimental test of the ICHH that includes manipulations of both hormones and infections in males of the territorial damselfly, Hetaerina americana, with accurate survival measurements. We conducted a fully factorial experiment subjecting each individual to one of three topical treatments: methoprene (a juvenile hormone analog), acetone, or control, and one of three injection treatments: bacteria, PBS, or control. We measured survival of manipulated males in both the wild and in captivity. As predicted, survival was most heavily impaired in methoprene‐bacteria males than in the other groups in the wild, and no survival differences emerged in captive animals. This result confirms that survival is one cost an animal pays for increased hormonal levels. This corroborates theoretical predictions of the ICHH.     

Corticosterone suppresses immune activity in territorial Galápagos marine iguanas during reproduction

Individuals that display elaborate sexually selected characters often show reduced immune function. According to the immunocompetence handicap hypothesis, testosterone (T) is responsible for this result as it drives the development and maintenance of sexual characters and causes immunosuppression. But glucocorticoids also have strong influences on immune function and may also be elevated in reproductively active males. Here, we compared immune activity using the phytohemagglutinin (PHA) skin test in three discrete groups of male marine iguanas (Amblyrhynchus cristatus): territorials, satellites, and bachelors. Males of these three reproductive phenotypes had indistinguishable T concentrations during the height of the breeding season, but their corticosterone (cort) concentrations, body condition and hematocrit were significantly different. Territorial males, the animals with the most elaborate sexual ornaments and behaviors, had lower immune responses and body condition but higher cort concentrations and hematocrit than satellites or bachelors. To test directly cort's immunosuppressive role, we elevated cort by either restraining animals or additionally injecting cort and compared their PHA swelling response with the response of free-roaming animals. Such experimental elevation of cort significantly decreased immune activity in both restrained and cort-injected animals. Our data show that cort can induce immunosuppression, but they do not support the immunocompetence handicap hypothesis in its narrow sense because T concentrations were not related to immunosuppression.     

Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent

The immunocompetence handicap hypothesis proposes that the immunosuppressive effect of testosterone enforces honesty of sexual signalling via a physiological trade-off between signal intensity and immunocompetence. However, evidence that testosterone is immunosuppressive is scant, particularly in birds. I studied the correlation between immunocompetence and testosterone in superb fairy-wrens (Malurus cyaneus), a species with intense intersexual selection. Males are seasonally dichromatic and testosterone increases during the moult from dull brown eclipse plumage into bright nuptial plumage. I determined the primary antibody response to immunization with sheep red blood cells (SRBCs) in (i) control and testosterone-implanted males in captivity, and (ii) a cross-section of free-living males with basal and elevated testosterone (in eclipse plumage, moulting and in nuptial plumage). Experimental treatment with testosterone decreased the likelihood of an antibody response to SRBCs in captive birds. In contrast, free-living males which had acquired the nuptial plumage and had naturally elevated testosterone were more likely to respond to SRBCs than males in eclipse plumage with basal testosterone levels. The association between higher immunocompetence and higher immunosuppressive testosterone could arise if both are positively correlated with male phenotypic quality In addition, the association could result if males compensate for potential immunosuppression by enhancing their humoral immune responses, particularly since high testosterone is linked to other demanding activities such as moulting and courtship displays.     

Experimentally increased social competition compromises humoral immune responses in house finches

Although social behavior can substantially influence an individual's physiology, few studies have examined whether intraspecific competition compromises individual immunocompetence. We experimentally manipulated the intensity of social competition in captive non-breeding house finches (Carpodacus mexicanus) by supplying few (high competition) or many (low competition) feeding sites. We tested whether elevated levels of social competition caused individual changes in aggression rates, humoral immunity, body mass, and baseline and stress-induced corticosterone concentrations. We also examined whether physiological responses to social competition were related to an individual's social status. We found that house finches under high social competition had significantly higher aggression rates, lower antibody responses, and lost more body mass. Within flocks, dominant individuals mounted stronger immune responses in both competition treatments. Our statistical power to detect differences in circulating corticosterone concentrations was low, but we did not find any support for the hypothesis that corticosterone concentrations mediate immunosuppression among or within flocks: baseline and stress-induced corticosterone concentrations did not differ under high and low social competition, were unrelated to individual social status, and did not predict the extent of immunosuppression among individuals. Overall, we documented that two universal components of social behavior, intraspecific competition and social status, modulated the strength of a humoral immune response in house finches.     

Patterns of breeding behaviour and plasma levels of hormones in a free-living population of Pied flycatchers, Ficedula hypoleuca

Plasma levels of luteinizing hormone (LH) and steroid hormones were measured by radioimmunoassay in a series of plasma samples collected from a free-living population of Pied flycatchers, Ficedula hypoleuca. Both males and females have similar circulating levels of LH and testosterone when they arrive in the breeding area. However, as territories and pair bonds are established, and as courtship and nest-building ensue, the plasma levels of testosterone in males become elevated over those of females, although a lesser peak also occurs in females. As the egg laying phase and incubation begin, plasma levels of LH and testosterone decline sharply in both sexes. On the other hand polyterritorial males, that establish secondary territories, maintain higher levels of LH and testosterone than males remaining in the home-territory, at least until they return to the home-territory, usually at the middle part of the incubation period. By this time polyterritorial males also have basal levels of these hormones. Curiously, females on home-territories show a small, but significant, rise of circulating LH and testosterone at the time the males return.
In males, plasma levels of corticosterone are elevated from the time of arrival on the breeding grounds until the end of the nest-building period. Thereafter corticosterone levels decline in males staying on the home-territory but remain elevated in polyterritorial males until the latter return to the home-territory. In contrast, circulating levels of corticosterone in females are only elevated for brief period during egg laying.     

Honest signals and sexual conflict: Female lizards carry undesirable indicators of quality

Sex differences in animal coloration often result from sex‐dependent regulatory mechanisms. Still, some species exhibit incomplete sexual dimorphism as females carry a rudimentary version of a costly male trait, leading to intralocus sexual conflict. The underlying physiology and condition dependence of these traits can inform why such conflicts remain unresolved. In eastern fence lizards (Sceloporus undulatus), blue iridophore badges are found in males and females, but melanin pigmentation underneath and surrounding badges is male‐exclusive. We track color saturation and area of badges across sexual maturity, and their relationship to individual quality (body condition and immunocompetence) and relevant hormones (testosterone and corticosterone). Saturation and testosterone were positively correlated in both sexes, but hormone and trait had little overlap between males and females. Saturation was correlated with body condition and immunocompetence in males but not in females. Co‐regulation by androgens may have released females from resource allocation costs of color saturation, even when in high condition. Badge area was independent of testosterone, but associated with low corticosterone in females, indicating that a nonsex hormone underlies incomplete sexual dimorphism. Given the evidence in this species for female reproductive costs associated with ornamentation, this sex‐nonspecific regulation of an honest signal may underlie intralocus sexual conflict.     

外源性皮质酮对雄性根田鼠交配行为的作用

本文研究了皮质酮对雄性根田鼠交配行为的作用。实验个体分别注射0.10 ug/ g体重、0. 60 ug / g体重和1.00 ug/ g体重剂量的皮质酮,1 h后测定每只雄性根田鼠的交配行为。结果显示,3 个处理组动物具有射精能力的个体比率及其爬跨、抽动和射精潜伏期与对照组动物相比均无显著差异,爬跨和抽动频次也无显著变化。不同处理组个体的血浆睾酮含量无显著差异。因此,皮质酮没有影响雄性根田鼠的交配行为和性激素的分泌。该结果提示,哺乳动物在急性应激条件下所分泌的皮质酮可能不参与对性行为的调控。     

Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent

Animals have to adjust their physiology to seasonal changes, in response to variation in food availability, social tactics and reproduction. I compared basal corticosterone and testosterone levels in free ranging striped mouse from a desert habitat, comparing between the sexes, breeding and philopatric non-breeding individuals, and between the breeding and the non-breeding season. I expected differences between breeders and non-breeders and between seasons with high and low food availability. Basal serum corticosterone was measured from 132 different individuals and serum testosterone from 176 different individuals of free living striped mice. Corticosterone and testosterone levels were independent of age, body weight and not influenced by carrying a transmitter. The levels of corticosterone and testosterone declined by approximately 50% from the breeding to the non-breeding season in breeding females as well as non-breeding males and females. In contrast, breeding males showed much lower corticosterone levels during the breeding season than all other classes, and were the only class that showed an increase of corticosterone from the breeding to the non-breeding season. As a result, breeding males had similar corticosterone levels as other social classes during the non-breeding season. During the breeding season, breeding males had much higher testosterone levels than other classes, which decreased significantly from the breeding to the non-breeding season. My results support the prediction that corticosterone decreases during periods of low food abundance. Variation in the pattern of hormonal secretion in striped mice might assist them to cope with seasonal changes in energy demand in a desert habitat.     

Corticosterone,testosterone and life-history strategies of birds

Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.     

Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia

A group of 10 territorial male song sparrows, Melospiza melodia, were given subcutaneous implants of corticosterone in Silastic tubing. A second group of 10 territorial males were given empty implants as controls. After 18-24 hr all males were then subjected to a simulated territorial intrusion (STI) by placing a caged male song sparrow in the center of the subject's territory, and playing tape recorded songs through a speaker placed alongside. Significantly fewer males with corticosterone implants responded to STI than to controls, and the latency to respond was longer. Of the 3 experimental males that did respond to STI, all had a lower frequency of songs and did not approach the simulated intruder as closely as controls. Many males were captured 2-7 days after implantation and blood samples collected for measurement of circulating hormone levels. As expected, plasma levels of corticosterone were high in the group given corticosterone implants. However, plasma levels of luteinizing hormone (LH) were not affected by treatment with corticosterone, and although circulating levels of testosterone were depressed slightly compared with controls, they were within the normal range for territorial and breeding males. There were no differences in body mass despite greatly increased fat depots in males treated with corticosterone. These data suggest that high levels of corticosterone, similar to those measured during stressful episodes both in the laboratory and field, may suppress territorial behavior independently of the adenohypophysial-gonad axis. Since plasma levels of LH and testosterone are not depressed markedly, thus maintaining the gonads in a near functional state, renesting can begin as soon as environmental conditions ameliorate. Such mechanisms could potentially increase the probability of raising viable young after unpredictable, severe weather resulted in failure of the previous breeding attempt.     

Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus

Over a 2-yr period, we investigated the annual cycles of plasma testosterone and corticosterone and the relationships between these hormones and body condition in a wild population of male red-spotted garter snakes, Thamnophis sirtalis concinnus. In the 10 mo that were sampled, a peak in testosterone was observed in late summer during gametogenesis and declining through the spring breeding period. Corticosterone and testosterone cycles were positively correlated, in contrast to many vertebrates, suggesting the lack of a direct negative interaction between the two hormones. Body condition, defined as the residual of the regression of mass on snout-vent length, also cycled annually, with individuals being more robust during the summer than during the spring or fall. Individuals with a positive body condition had significantly lower plasma levels of corticosterone than did individuals with a negative body condition, supporting the energetic role of glucocorticoids. There was no relationship between body condition and testosterone. This study suggests that annual cycles of testosterone, corticosterone, and body condition can be associated with one another, and considering all three simultaneously is necessary to understand their control and function.     

Oral immunogenicity of tomato-derived sDPT polypeptide containing Corynebacterium diphtheriae, Bordetella pertussis and Clostridium tetani exotoxin epitopes

DPT vaccine, designed to immunize against diphtheria, pertussis, and tetanus, has been shown to be effective in humans. Nevertheless, dissatisfaction with the whole-cell preparations is due to the reactogenicity, which has to lead to the development of new safer formulations. Previously, we described the expression in tomato of a plant-optimized synthetic gene encoding the recombinant polypeptide sDPT, containing mainly immunoprotective epitopes of the diphtheria, pertussis and tetanus exotoxins and two adjuvants. In this study, we examined whether the ingestion of tomato-derived sDPT protein induces specific antibodies in mice after three weekly doses scheme. A positive group immunized with DPT toxoids was included. Specific antibody levels were assessed in serum, gut and lung. Sera tested for IgG antibody response to pertussis, tetanus and diphtheria toxin showed responses to the foreign antigens; interestingly, the response to diphtheria epitope was similar to those observed in the positive group. We found higher IgG1 than IgG2a responses in serum. A modest IgG response was observed in the tracheopulmonary fluid. High response of IgA against tetanus toxin was evident in gut, which was statistically comparable to that obtained in the positive group. The levels of response in these groups were higher than those in mice that received wild-type tomato. These findings support the concept of using transgenic tomatoes expressing sDPT polypeptide as model for edible vaccine against diphtheria, pertussis, and tetanus.     

Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog

We investigated physiological constraints on calling behaviour in the túgara frog, Physalaemus pustulosus. First, we examined the hypothesis that energetic factors limit calling. Time spent in chorus activity is the best predictor of male mating success (Ryan, 1985). Manipulation of food availability demonstrated that males given supplemental food were more likely to call than males without supplemental food. Males without supplemental food were less likely to call even though their lipid reserves were only slightly less than males given the supplemental food, suggesting that part of the increased energy obtained from the supplemental food may have been channelled into calling to attract females. Secondly, we examined the role of steroid hormones in switching between reproductive and non-reproductive behaviours. Calling males had higher levels of plasma testosterone than silent males. Experimental elevation of corticosterone decreased testosterone levels and the likelihood of calling, thus linking both of these steroid hormones to calling behaviour. Males who responded to supplemental food by increasing calling had higher levels of testosterone than those without supplemental food, but there was no difference in plasma corticosterone levels. Overall, the results suggest that energetic factors affect calling behaviour and that one potential mechanism for this affect is through plasma testosterone levels. Corticosterone can decrease calling behaviour, however, corticosterone does not appear to mediate the effect of energetic factors on calling behaviour. These data are consistent with the hypothesis that energetic factors ultimately constrain sexual selection for calling behaviour.     

Mounting an immune response correlates with decreased androgen levels in male peafowl, <Emphasis Type="Italic">Pavo cristatus</Emphasis>

Studies testing the “immunocompetence handicap hypothesis” have focussed on the immunosuppressive effects of androgens. Several recent studies have reported that mounting a humoral immune response might also result in a decrease in circulating androgen levels via a “negative feedback” on the hypothalamus–pituitary–gonadal axis (HPG). The aim of this correlative study was to analyse these immunosuppressive and HPG-suppressive interactions in reproductively active males of the peafowl. We collected blood samples of free living birds before and after challenging the immune system with a non-pathogenic antigen (sheep erythrocytes), and analysed immune parameters and plasma levels of the two main androgens in birds, testosterone and dihydrotestosterone. Males displaying larger versions of the main secondary sexual trait, the long and conspicuously ornamented train, tended to have higher androgen levels and significantly lower circulating levels of leukocytes, indicating that exaggerated ornaments might signal properties of the endocrine and immune system. Actual circulating levels of androgens did not correlate with the plasma levels of leukocytes and the antibody response to SRBC. However, changes in plasma levels of both androgens showed negative correlation with both leukocytes (P < 0.1) and SRBC responses (P < 0.05). The data therefore support the prediction that activity of the immune system is HPG-suppressive. Such suppression has been proposed to be especially costly during the reproductive season, during which androgens facilitate the expression of exaggerated traits that play an important role in sexual competition.