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.     

Melanin-based coloration and immunity in polymorphic population of pied flycatcher, <Emphasis Type="Italic">Ficedula hypoleuca</Emphasis>

A specific interest in the persistence of color polymorphism in some populations of birds and other vertebrates is often linked to ideas about the signaling honesty of bright coloration. The evolution of conspicuous ornamentation could be associated with physiological costs including limitations of the immune system. The study of this process is crucial for an understanding of the maintenance of polymorphic coloration. Here we summarized the results of a study of a pied flycatcher population from the Moscow region (Russia) in 2010–2013. We experimentally induced antibody production by injecting sheep red blood cells (SRBC) and inflammatory swelling by injecting phytohaemagglutinin (PHA) after which we estimated the immune response in breeding males. We used leucocytes-to-erythrocytes and heterophils-to-lymphocytes (H/L) ratios as indicators of infectious, inflammatory processes and stress. The results showed that the feeding rates of males treated with SRBC decreased and negatively related to the intensity of their immune responses. Non-molting males of different color types did not significantly differ in antibody production. Among molting breeders, the immune response to SRBC was significantly higher in pale males than in bright ones with rich melanin-based coloration. In contrast to non-molting males, molting pale males had an increased antibody titer after immunization. The lower humoral immune response was associated with the higher H/L stress index before immunization. The change in H/L after immunization positively correlated with the intensity of the humoral immune response. As opposed to humoral immunity, we did not find any significant predictors, including coloration, molt, or their two-way interaction, to explain the variation in cutaneous inflammatory response to PHA. The results suggest that the apparent advantage of a cryptic male phenotype over a conspicuous phenotype occurring in one of two types of immune response has an impact on the maintenance of color polymorphism in the pied flycatcher.     

Androgen levels and female social dominance in Lemur catta

Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are influenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and conflict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming effects for a complete understanding of this phenomenon.     

Low Testosterone Correlates with Delayed Development in Male Orangutans

Male orangutans (Pongo spp.) display an unusual characteristic for mammals in that some adult males advance quickly to full secondary sexual development while others can remain in an adolescent-like form for a decade or more past the age of sexual maturity. Remarkably little is understood about how and why differences in developmental timing occur. While fully-developed males are known to produce higher androgen levels than arrested males, the longer-term role of steroid hormones in male life history variation has not been examined. We examined variation in testosterone and cortisol production among 18 fully-developed (“flanged”) male orangutans in U.S. captive facilities. Our study revealed that while testosterone levels did not vary significantly according to current age, housing condition, and species origin, males that had undergone precocious development had higher testosterone levels than males that had experienced developmental arrest. While androgen variation had previously been viewed as a state-dependent characteristic of male developmental status, our study reveals that differences in the physiology of early and late developing males are detectable long past the developmental transition and may instead be trait-level characteristics associated with a male’s life history strategy. Further studies are needed to determine how early in life differences in testosterone levels emerge and what consequences this variation may have for male behavioral strategies.     

三个地方鸡种MHC B-L BII基因遗传变异与免疫性状的关联分析

旨在研究3个地方鸡品种(汶上芦花鸡、莱芜黑鸡、济宁百日鸡)主要组织相容性复合体(Major Histocompatibility Complex,MHC) B-LBII基因遗传变异与绵羊红细胞(Sheep red blood cell,SRBC)、禽流感(Avian influenza,AI)和新城疫(Newcastle disease,ND)抗体滴度等免疫性状的关系,揭示不同品种间基因变异与免疫性状的相关性.以300只地方品种鸡为材料,运用直接测序和聚合酶链式反应-单链构象多态性(PCR-SSCP)等技术检测MHC B-L BⅡ基因的序列变异.在3个地方鸡品种中分别发现了19～22个核苷酸变异位点,可导致其中16～18个氨基酸的变异.3个地方鸡种MHC B-L BⅡ基因中分别有7～8个(Single nucleotide polymorphism,SNP)位点与部分免疫性状存在不同程度的显著相关性.变异位点G97A和T138A在3个品种中均存在,与SRBC、ND、AI抗体滴度均显著相关(P＜0.05).其中,G97A突变在济宁百日鸡中与ND抗体滴度显著相关(P＜0.05),在莱芜黑鸡中与SRBC抗体滴度显著相关(P＜0.05),在汶上芦花鸡中与H9抗体滴度显著相关(P＜0.05);变异位点T138A在汶上芦花鸡和济宁百日鸡中与H9抗体滴度显著相关(P＜0.05).研究表明3个地方鸡种的MHC B-LBII基因遗传变异与免疫性状存在显著关联.     

Hormonal correlates of social status and courtship display in the cooperatively lekking lance-tailed manakin

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations.     

Intra-sexual variation in male reproduction in teleost fish: a comparative approach

The occurrence of intra-sexual variation in reproduction is a widespread phenomenon in teleosts. One such form of variation consists in the occurrence of alternative male types: males that invest resources in mate attraction and males that exploit the investment of the former males, by trying to sneak fertilizations during spawning. These alternative reproductive tactics can be classified according to their plasticity during the life span of the individuals (i.e., fixed vs. sequential vs. reversible). Furthermore, the differences between morphs within a given species may involve a set of different traits, including reproductive behavior, the differentiation of male morphological traits, and the patterns of gonad tissue allocation and the differentiation of gonadal accessory glands. In this paper, we review the available data on four species exhibiting different types of intra-sexual plasticity in reproduction that have been studied in our lab. The data on the proximate mechanisms, androgens and forebrain arginine-vasotocin (AVT), underlying these alternative tactics suggest that between-morph differences in androgen levels, especially in 11-ketotestosterone, are especially present in species where the alternative male types have evolved morphological traits that are tactic-specific (i.e., sexual polymorphisms) and that differences in AVT appear to be related to between-morph differences in the expression of courtship behavior. Therefore, this comparative approach leads us to propose that the different endocrine systems are involved in the differentiation of different sets of traits that make up alternative phenotypes, and that the differentiation of alternative tactics is not controlled by a single endocrine system (e.g., androgens).     

Immune responses during measles infection in immunosuppressed Rhesus monkeys.

Rhesus monkeys immunosuppressed with horse anti-human thymocyte gamma-globulin (ATG) were infected with measles and simultaneously inoculated with sheep erythrocytes (SRBC), a thymus-dependent antigen, and with pneumococcal polysaccaride type III (SSS-III), a thymus-independent antigen. ATG treatment alone suppressed SRBC antibody production, had no effect on SSS-III antibody production, and effectively eliminated circulating T cells compared to nonsuppressed monkeys. ATG treatment of measles-infected monkeys resulted in delayed virus clearance and delayed antibody production compared to nonsuppressed infected monkeys. After cessation of ATG treatment, measles antibodies and T cells reached normal levels, and measles virus was eliminated. Thus, immune clearance of measles virus is T cell-dependent, but the relative roles of cellular- and humoral-mediated immunity in vivo could not be clearly separated. Also, measles infection was associated with a decreased T cell mitogen responsiveness of circulating lymphocytes but not of lymph node lymphocytes, suggesting an altered circulating pattern of the cells responsible for delayed hypersensitivity. Also, measles infection had no effect on T-dependent antibody production to SRBC.     

Managing anabolic steroids in pre-hibernating Arctic ground squirrels: obtaining their benefits and avoiding their costs

Androgens have benefits, such as promoting muscle growth, but also significant costs, including suppression of immune function. In many species, these trade-offs in androgen action are reflected in regulated androgen production, which is typically highest only in reproductive males. However, all non-reproductive Arctic ground squirrels, irrespective of age and sex, have high levels of androgens prior to hibernating at sub-zero temperatures. Androgens appear to be required to make muscle in summer, which, together with lipid, is then catabolized during overwinter. By contrast, most hibernating mammals catabolize only lipid. We tested the hypothesis that androgen action is selectively enhanced in Arctic ground squirrel muscle because of an upregulation of androgen receptors (ARs). Using Western blot analysis, we found that Arctic ground squirrels have AR in skeletal muscle more than four times that of Columbian ground squirrels, a related southern species that overwinters at approximately 0°C and has low pre-hibernation androgen levels. By contrast, AR in lymph nodes was equivalent in both species. Brain AR was also modestly but significantly increased in Arctic ground squirrel relative to Columbian ground squirrel. These results are consistent with the hypothesis that tissue-specific AR regulation prior to hibernation provides a mechanism whereby Arctic ground squirrels obtain the life-history benefits and mitigate the costs associated with high androgen production.     

Stress hormone is implicated in satellite-caller associations and sexual selection in the Great Plains toad

The effects of androgens on male-typical traits suggest that variation among males in circulating levels can play a major role in sexual selection. We examined whether variation in vocal attractiveness is attributable to differences in androgen levels among Great Plains toads (Bufo cognatus). We found that noncalling "satellite" males practicing an alternative mating tactic were more likely to associate with males producing long calls. However, callers with satellites did not have higher androgen levels than callers without satellites. Rather, callers with satellites had significantly lower corticosterone (CORT) levels than callers without satellites. A CORT manipulation experiment suggested that differences in calls for males with and without satellites were related to differences in CORT levels. Furthermore, there was a negative correlation between CORT level and call duration within most nights of chorus activity. However, the correlation was weak for the pooled data (across all nights), suggesting that local environmental and/or social factors also affect call duration. Last, we show that females preferred broadcast calls of longer duration, characteristic of males with satellites and low CORT. These results imply that satellites optimize their reproductive success by associating with males producing long calls. However, this association should negatively affect the fitness of attractive callers.     

Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi)

Exposure to androgens during prenatal development shapes both physiological and behavioral developmental trajectories. Notably, in rhesus macaques, prenatal androgen exposure has been shown to increase rough-and-tumble play, a prominent behavioral feature in males during the juvenile period in primates. While macaques are an Old World, polygamous species with marked sexually dimorphic behavior, New World callitrichine primates (marmosets and tamarins) live in cooperative breeding groups and are considered to be socially monogamous and exhibit minimal sexual dimorphism in social play, which suggests that androgen may affect this species in different ways compared to macaques. In addition, we previously described considerable variation in maternal androgen production during gestation in marmosets. Here we tested the association between this variation and variation in offspring rough-and-tumble play patterns in both males and females. We measured testosterone and androstenedione levels in urine samples collected from pregnant marmoset mothers and then observed their offspring's play behavior as juveniles (5-10 months of age). In contrast to findings in rhesus macaques, hierarchical regression analyses showed that higher gestational testosterone levels, primarily in the second semester, were associated with decreased rough-and-tumble play in juveniles, and this relationship appears to be driven more so by males than females. We found no reliable associations between gestational androstenedione and juvenile play behavior. Our findings provide evidence to suggest that normative variation in levels of maternal androgen during gestation may influence developmental behavioral trajectories in marmosets in a way that contradicts previous findings in Old World primates.     

Constitutive immune defences correlate with life-history variables in tropical birds

1. It has been suggested that immune defences are shaped by life history and ecology, but few general patterns have been described across species. We hypothesized that 'fast' life-history traits (e.g. short development times, large clutch sizes) would be associated with developmentally inexpensive immune defences, minimizing the resource demands of young animals' immune systems during periods of rapid growth. Conversely, 'slow' life histories should be associated with well developed antibody-mediated defences, which are developmentally costly. 2. We therefore predicted that 'fast-living' species would exhibit higher levels of complement proteins, a component of non-specific innate defence, but lower levels of constitutive ('natural') antibodies. Additionally, we predicted that constitutive immune defences in general would be higher in species with ecological characteristics that might increase exposure to pathogens, such as open nests, omnivorous diets, gregariousness, and closed forested habitat. 3. Across 70 Neotropical bird species, we found a strongly positive relationship between incubation period and natural antibody levels in adult birds, suggesting that longer developmental times might allow the production of a more diverse and/or more reactive adaptive immune system. Complement activity was positively, although weakly, correlated with clutch size, providing some support for the hypothesis that faster-living species rely more on innate defences, such as complement. Unexpectedly, solitary species had higher natural antibody titres than species that frequently join flocks. 4. Our results suggest that, despite probably widespread differences in the intensity and diversity of pathogen exposure, species-level variation in constitutive immune defences is understandable within the context of life-history theory.     

Tight hormonal phenotypic integration ensures honesty of the electric signal of male and female Brachyhypopomus gauderio

Hormones mediate sexually selected traits including advertisement signals. Hormonal co-regulation links the signal to other hormonally-mediated traits such that the tighter the integration, the more reliable the signal is as a predictor of those other traits. Androgen administration increases the duration of the communication signal pulse in both sexes of the electric fish Brachyhypopomus gauderio. To determine whether the duration of the signal pulse could function as an honest indicator of androgen levels and other androgen-mediated traits, we measured the variation in sex steroids, signal pulse duration, and sexual development throughout the breeding season of B. gauderio in marshes in Uruguay. Although the sexes had different hormone titres and signal characteristics, in both sexes circulating levels of the androgens testosterone (T) and 11-ketotestosterone (11-KT) were strongly related to signal pulse duration. Consequently, signal pulse duration can serve as an honest indicator of circulating androgens in males and females alike. Additionally, through phenotypic integration, signal pulse duration also predicts other sexual traits directly related to androgen production: gonad size in males and estradiol (E2) levels in females. Our findings show that tight hormonal phenotypic integration between advertisement signal and other sex steroid-mediated traits renders the advertisement signal an honest indicator of a suite of reproductive traits.     

Anti-IgD enhancement of primary antibody responses in rats

The role of membrane IgD in immune responses was examined by treating adult rats with anti-IgD. Anti-IgD when administered to rats in conjunction with optimal or suboptimal doses of either SRBC, a T-dependent antigen, or DNP-Ficoll, a T-independent antigen, enhanced the antibody responses. The greatest enhancement was obtained when anti-IgD was administered before the antigen. The effects of anti-IgD on antibody responses to SRBC were: (i) significant antibody responses to suboptimal antigen concentrations; (ii) greater antibody responses to optimal antigen concentrations; (iii) accelerated antibody responses; (iv) an early shift from IgM to IgG antibodies; (v) prolonged antibody responses. Similar effects on the immune response to DNP-Ficoll were observed with the exception that all antibodies were 2ME sensitive (IgM). These results suggest that an anamnestic type of immune response can be induced in anti-IgD-treated rats when given a primary antigen exposure. Injection of anti-IgD without SRBC or DNP-Ficoll induces B-cell proliferation without detectable antibody production to these antigens, indicating at least two signals are required for the enhanced antibody responses.     

Sex steroid hormones enhance immune function in male and female Siberian hamsters

Immune function is better in females than in males of many vertebrate species, and this dimorphism has been attributed to the presence of immunosuppressive androgens in males. We investigated the influence of sex steroid hormones on immune function in male and female Siberian hamsters. Previous studies indicated that immune function was impaired in male and female hamsters housed under short-day photoperiods when androgen and estrogen concentrations were virtually undetectable. In experiment 1, animals were gonadally intact, gonadectomized (gx), or gx with hormone replacement. Females exhibited the expected increase in antibody production over males, independent of hormone treatment condition, whereas male and female gx animals exhibited decreased lymphocyte proliferation to the T cell mitogen, phytohemagglutinin (PHA) compared with intact animals, and this effect was reversed in gx hamsters following testosterone and estradiol treatment, respectively. In experiment 2, testosterone, dihydrotestosterone, and estradiol all enhanced cell-mediated immunity in vitro, suggesting that sex steroid hormones may be enhancing immune function through direct actions on immune cells. In experiment 3, an acute mitogen challenge of lipopolysaccharide significantly suppressed lymphocyte proliferation to PHA in intact males but not females, suggesting that males may be less reactive to a subsequent mitogenic challenge than females. Contrary to evidence in many species such as rats, mice, and humans, these data suggest that sex steroid hormones enhance immunity in both male and female Siberian hamsters.     

Androgens and Immune Function in Male Alternative Reproductive Morphotypes of the Peacock Blenny Salaria pavo

Species with alternative reproductive tactics offer the opportunity to analyse how behavioural and morphological traits are tuned to produce successfully competing phenotypes within one sex. In the teleost fish Salaria pavo , alternative reproductive tactics are sequential. The older ornamented males compete for access to females by guarding a cavity to which they attract females to spawn. Ornamented males that are found without a nest are called 'floaters'. Younger mature males which are too small to compete with nest-holders attempt to 'sneak' as female mimics into successful nests and release their sperm to fertilize freshly spawned eggs. The alternative tactics in S. pavo are associated with different levels of the androgens testosterone and 11-ketotestosterone, which have been found to suppress immune function in several teleost fish. A field study was carried out to analyse the relationship between these reproductive tactics, androgens and blood levels of lymphocytes as a monitoring method of immune function. We expected highest investment in the immune system in sneakers because these have the lowest androgen levels and functionally because investing in self-maintenance increases their future prospect to switch tactic and to reproduce as a nest-holder. Indeed, the relative count of lymphocytes correlated negatively with body size and thus was highest in sneakers and lowest in nest-holders. In concordance, 11-ketotestosterone and testosterone levels were found to be higher in floaters and nest-holders than in sneakers. However, no correlation was found between individual levels of testosterone or 11-ketotestosterone and lymphocytes. Thus, a trade-off between reproductive traits associated with high androgen levels and immunocompetence might exist at the level of alternative tactics but this might not be explained by acute immunosuppressive effects of circulating androgens.     

Trade-offs between immune investment and sexual signaling in male mallards

Allocation trade-offs between the immune system and sexual traits are central to current sexual selection hypotheses but remain contentious. Such trade-offs could be brought about by the dual action of testosterone that stimulates sexual signals but also suppresses immune functions and/or by competition for carotenoids that can be deposited in ornaments or used as antioxidants in support of immune functions. We investigated the trade-off between investment in immunity and maintenance of testosterone, carotenoids, and sexually selected, carotenoid-based bill color in male mallards. Following a nonpathogenic immune challenge, facultative immune investment resulted in a syndrome of changes in allocation. Plasma carotenoids disappeared from circulation proportional to antibody production. In addition, the reflectance spectrum of the bill was affected; greater antibody production was associated with an increase in relative UV reflectance. Although changes in bill reflectance and plasma carotenoids were related, the relationship appeared more complex than direct competition with immunity. Finally, maintenance of testosterone was affected by immune investment: testosterone levels declined substantially when males produced more antibodies. Because males with high testosterone are preferred by females, the decline in testosterone, in addition to carotenoid depletion and effects on bill reflectance, could constitute a significant cost of immune investment.     

The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow

Variation in immune responses is an important part of life history variation. When correlations between multiple immune measures are reported, studies report different patterns. I tested whether the correlation between levels of immune response was consistent across a species range. The ability of tree swallows Tachycineta bicolor to simultaneously produce immune responses to both a humoral immune response and T-cell mediated local inflammation to PHA was tested at three sites that span the breeding range. Females in Tennessee maintained stronger PHA responses than did females in either New York or Alaska. In New York and Alaska, individuals that produced strong PHA responses produced low levels of antibodies to a humoral challenge of sheep red blood cells (SRBC). However, in Tennessee, individuals that showed strong local PHA inflammation also mounted strong responses to SRBC. Increasing daily daytime temperatures led to increased PHA response, but there were no differences in the effect of temperature among sites. These results indicate spatial and/or temporal variation occurs in the ability to produce multiple immune responses simultaneously; this pattern suggests important geographic (or temporal) differences in factors driving investment in immune activity. In addition, these results suggest that studies extrapolating results across populations should be careful to consider geographic variation in immune activity.     

The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes

Many sexually selected traits in male fishes are controlled by testosterone. Directional selection for male ornaments could theoretically increase male testosterone levels over evolutionary timescales, and when genetically correlated, female testosterone levels as well. Because of the negative fitness consequences of high testosterone, it is plausible that female choice for sexually selected traits in males results in decreased female reproductive fitness. I used comparative analysis to examine the association between male peak testosterone expression and sexually selected ornaments. I also tested for genetic correlation between male and female androgen levels. The presence of sexually selected traits in males was significantly correlated with increased peak androgen levels in males as well as females, and female testosterone levels were significantly correlated with male peak testosterone titers, although the slope was only marginally <1. This suggests that selection to decouple high male and female testosterone levels is either weak or otherwise ineffective.     

Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism

Current theory recognizes the adaptive value of maternal effects in shaping offspring phenotypes in response to selective pressures and vindicates the value of these traits in fostering adaptation and speciation. Yolk androgens in birds are a relatively well-known maternal effect and have been linked to adaptations related to development, coloniality life, and sexual selection. We tested whether interspecific patterns of yolk androgen levels (androstenedione and testosterone) were related to interspecific variation in development, sexual selection, and coloniality. First, we found no relationship between androgen levels and duration of development as reflected by incubation and nestling periods. However, androstenedione concentration was positively related to the relative duration of the incubation period and negatively related to the relative duration of the nestling period. These relationships were confirmed by analyses of phylogenetically independent contrasts. We suggest that androstenedione concentration may have evolved as a mechanism to shift the relative duration of development between the egg and nestling stages in response to selective pressures that differentially affect the duration of each stage. Second, neither plumage dichromatism nor mating system explained significant variation in yolk androgen levels after correction for similarity among species due to common descent. This finding indicates that sexual selection has not been an important selective pressure for this maternal effect. Third, we found a highly significant positive relationship between degree of breeding coloniality and concentration of androstenedione but not testosterone. These effects were confirmed in analyses of contrasts controlling for similarity due to common descent. Since the relationship with coloniality was different for each androgen, it is unlikely that increased levels of androgens in highly colonial species are a mere consequence of elevated androgen levels in mothers. Rather, our results suggest that high levels of androstenedione in eggs of colonial species are an adaptation to colony life, possibly related to the production of highly competitive phenotypes. In conclusion, from a comparative perspective, the results of this study support the role of maternal effects in promoting adaptation to certain environmental pressures.