Immunocompetence Handicap Hypothesis Research Articles

Ecological immunology: do sexual attraction and immunity trade-off through a desaturase?

Given the limited availability of resources in nature, sexual attractiveness may trade off with immunocompetence, as the immunocompetence handicap hypothesis (ICHH) posits. In invertebrates, a direct link between trade-offs through hormonal/molecular effectors in sexual signals and immunity has not been found so far. Here, we assessed how variation in sexual signals affected parasite infection in two sex pheromone selected lines of the moth Chloridea virescens: an attractive line with a low ratio of 16:Ald/Z11-16:Ald and an unattractive line with a high ratio. When infecting these lines with an apicomplexan parasite, we found that the attractive Low line was significantly more susceptible to the parasite infection than the unattractive High line. Since the ratio difference between these two lines is determined by a delta-11-desturase, we hypothesized that this desaturase may have a dual role, i.e., in the quality of the sexual signal as well as an involvement in immune response, comparable to testosterone in vertebrates. However, when we used CRISPR/cas9 to knockout delta-11-desturase in the attractive Low line, we found that the pheromonal phenotype did change to that of the High line, but the infection susceptibility did not. Notably, when checking the genomic location of delta-11-desaturase in the C. virescens, we found that mucin is adjacent to delta-11-desaturase. When comparing the mucin sequences in both lines, we found four nonsynonymous SNPs in the coding sequence, as well as intronic variation between the two lines. These differences suggest that genetic hitchhiking may explain the variation in susceptibility to parasitic infection.

Complex effects of testosterone level on ectoparasite load in a ground squirrel: an experimental test for the immunocompetence handicap hypothesis

BackgroundThe immunocompetence handicap hypothesis suggests that males with a higher testosterone level should be better at developing male secondary traits, but at a cost of suppressed immune performance. As a result, we should expect that males with an increased testosterone level also possess a higher parasite load. However, previous empirical studies aimed to test this prediction have generated mixed results. Meanwhile, the effect of testosterone level on parasite load in female hosts remains poorly known.MethodsIn this study, we tested this prediction by manipulating testosterone level in Daurian ground squirrels (Spermophilus dauricus), a medium-sized rodent widely distributed in northeast Asia. S. dauricus is an important host of ticks and fleas and often viewed as a considerable reservoir of plague. Live-trapped S. dauricus were injected with either tea oil (control group) or testosterone (treatment group) and then released. A total of 10 days later, the rodents were recaptured and checked for ectoparasites. Fecal samples were also collected to measure testosterone level of each individual.ResultsWe found that testosterone manipulation and sex of hosts interacted to affect tick load. At the end of the experiment, male squirrels subjected to testosterone implantation had an averagely higher tick load than males from the control group. However, this pattern was not found in females. Moreover, testosterone manipulation did not significantly affect flea load in S. dauricus.ConclusionsOur results only lent limited support for the immunocompetence handicap hypothesis, suggesting that the role of testosterone on regulating parasite load is relatively complex, and may largely depend on parasite type and gender of hosts.Graphical

Tick-tock, racing the clock: parasitism is associated with decreased sprint performance in the Eastern fence lizard

Abstract Host–parasite relationships are important components of ecological systems that influence the evolution of both hosts and parasites. High levels of ectoparasitic infections can disrupt host homeostasis, causing adverse effects on health and performance. However, the effects of natural ectoparasite levels on host physiology are less understood, with most research designs implementing experimental or hormonal manipulations of hosts. In this study, we examined the interplay between tick parasitism and host characteristics on body condition and locomotor performance in Eastern fence lizards in natural settings. We found a higher frequency of tick infections in male lizards relative to females, with larger males being more likely to experience tick infection. Infected lizards had reduced locomotor performance, max sprint speed and 2-m run speed. Together this suggests an energetic trade-off between increased immune function and reduced locomotor performance, which is consistent with the immunocompetence–handicap hypothesis. Higher numbers of ticks on adult male lizards may be explained by age as well as the immunosuppressive effects of testosterone. Tick infection did not appear to reduce overall body condition of lizard hosts. Our findings shed light on the interplay between ectoparasitic infection, host characteristics, and locomotor performance under natural conditions. Such insights are crucial for understanding host–parasite dynamics and determining the trade-offs for hosts within ecological contexts.

Ivermectin decreases parasite load, testosterone, and potentially antler length in a group of captive red deer males (Cervus elaphus)

Secondary sex traits (SSTs) can favour males in intra-sexual competition, allowing females to reliably assess their quality. They can also be connected to other aspects of fitness, such as resistance to parasites and pathogens, as parasites have negative effects on the development of SSTs. Antlers are one of the most recognizable examples of SSTs whose development is regulated by testosterone and reflects the actual condition of the bearer. Elevated testosterone can exaggerate the size of SSTs while impairing the function of the immune system (“The Immunocompetence Handicap Hypothesis”) posing a trade-off between antler development and immune function. In this study, we experimentally manipulated the parasite load in captive red deer (Cervus elaphus) males with Ivermectin during antler development for two consecutive years. Expecting an inverse proportionality between parasite load and antler size, we hypothesized the treated deer to have larger antlers than the untreated ones. Our results showed that, following the immunocompetence handicap hypothesis, parasite load was positively associated with testosterone levels. However, the application of Ivermectin suppressed the parasite load of the treated animals but did not lead to the development of larger antlers. Instead, it significantly suppressed the concentration of testosterone in the treated animals, whilst the animals that had higher testosterone also had the highest parasite load. Our findings show that Ivermectin can potentially decrease the levels of testosterone and, consequently, antler size. These findings have important implications for the management of captive populations, especially in contexts where the development of large trophies is desired.

Androgen and prolactin manipulation do not induce changes in immunocompetence measures in a fish with male parental care.

Prolactin and 11-ketotestosterone (11-KT) are important reproductive hormones in fishes, which may also influence immunocompetence. The immunocompetence handicap hypothesisstates that higher androgen concentrations that support secondary sex traits are traded off against a decrease in immune system function. To test the relationships between these hormones and immunocompetence, we experimentally manipulated 11-ketotestosterone and prolactin in the freshwater fish, bluegill (Lepomis macrochirus) during parental care using implants that contained either 11-KT, prolactin, or an inert control. We vaccinated individuals to stimulate the acquired immune response, then measured immunocompetence as the number of granulocytes, lymphocytes and monocytes, and the expression of interleukin 8 in each sample. We did not observe any significant differences in the immune measures among the hormone treatments. Our results indicate that in bluegill, there is no trade-off between androgens or prolactin and immunocompetence.

Long-term sex-dependent inflammatory response of adult frogs to ammonium exposure during the larval stage

Among others, the global change involves a worldwide increase in cropland area, with the concomitant rise in nitrogenous fertilizer supplementation and species range alterations, including parasites and pathogens. As most animals rely on their immune systems against these infectious agents, studying the potential effects of nitrogenous compounds on animal immune response is vital to understand their susceptibility to infections under these altered circumstances. Being subjected to an alarming process of global declines, amphibians are the object of particular attention, given their sensitivity to these compounds, especially to ammonium. Moreover, whereas adults can actively avoid polluted patches, larvae are confined within their waterbodies, thus exposed to contaminants in it. In this work, we test whether chronic exposure to a sublethal dose of ammonium during the larval stage of Pelophylax perezi frogs, released from all contamination after metamorphosis, leads to impaired inflammatory response to phytohemagglutinin in adults. We also test whether such a response differs between agrosystem individuals as compared with conspecifics from natural habitats. We found negative carryover effects of chronic exposure of larvae to ammonium on adult inflammatory response, which could imply a greater susceptibility to pathogens and parasites. However, this damage is only true for males, which, according to the immunocompetence handicap hypothesis, could be a consequence of a testosterone-triggered impairment of male immune function. In disagreement with our prediction, however, we detected no differences in the inflammatory response of agrosystem frogs to phytohemagglutinin as compared with natural habitat conspecifics.

Immunoecology of Species with Alternative Reproductive Tactics and Strategies

Alternative reproductive tactics and strategies (ARTS) refer to polymorphic reproductive behaviours in which in addition to the usual two sexes, there are one or more alternative morphs, usually male, that have evolved the ability to circumvent direct intra-sexual competition. Each morph has its own morphological, ecological, developmental, behavioural, life-history, and physiological profile that shifts the balance between reproduction and self-maintenance, one aspect being immunity. Immunoecological work on species with ARTS, which is the topic of this review, is particularly interesting because the alternative morphs make it possible to separate the effects of sex per se from other factors that in other species are inextricably linked with sex. We first summarize the evolution, development, and maintenance of ARTS. We then review immunoecological hypotheses relevant to species with ARTS, dividing them into physiological, life-history, and ecological hypotheses. In context of these hypotheses, we critically review in detail all immunoecological studies we could find on species with ARTS. Several interesting patterns emerge. Oddly, there is a paucity of studies on insects, despite the many benefits that arise from working with insects: larger sample sizes, simple immune systems, and countless forms of alternative reproductive strategies and tactics. Of all the hypotheses considered, the immunocompetence handicap hypothesis has generated the greatest amount of work, but not necessarily the greatest level of understanding. Unfortunately, it is often used as a general guiding principle rather than a source of explicitly articulated predictions. Other hypotheses are usually considered a posteriori, but perhaps they should take centre stage. Whereas blanket concepts such as “immunocompetence” and “androgens” might be useful to develop a rationale, predictions need to be far more explicitly articulated. Integration so far has been a one-way street, with ecologists delving deeper into physiology, sometimes at the cost of ignoring their organisms’ evolutionary history and ecology. One possible useful framework is to divide ecological and evolutionary factors affecting immunity into those that stimulate the immune system, and those that depress it. Finally, the contributions of genomics to ecology are being increasingly recognized and sometimes applied to species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort, as there is no grandeur in the strict reductionist view of life.

The benefits of being dominant: health correlates of male social rank and age in a marmot.

The benefits of dominance may not come without costs, particularly for males. For example, the “immunocompetence handicap hypothesis” states that males with enhanced mating success allocate resources to enhance reproductive output at a cost to their current health, whereas the “resource quality hypothesis” predicts that high-ranking males may benefit from increased reproduction and good health. Whereas the predictions from each have been well tested in captive animals and in a variety of highly social primates, fewer studies have been carried out in free-living, facultatively social animals. Using adult male yellow-bellied marmots (Marmota flaviventer), we evaluated predictions of these hypotheses by examining the relationship between social rank and 2 health indicators—fecal glucocorticoid metabolite (FCM) levels, and neutrophil/lymphocyte (N/L) ratios—after accounting for variation explained by age, body mass, and seasonality. We found that higher-ranking males tended to have a lower N/L ratio (reflecting good health) than lower-ranking individuals, whereas FCM levels were not significantly related to rank. In addition, heavier male marmots had lower N/L ratios, whereas body mass was not associated with FCM levels. We also found that older adult males had lower FCM levels (reflecting less physiological stress) but higher N/L ratios than younger adults. Finally, we found that FCM levels decreased as the active season progressed and FCM levels were associated with the time of the day. Overall, our results suggest that socially-dominant male marmots enjoyed better, not worse health in terms of lower N/L ratios.

Associations between testosterone and immune activity in alligators depend on bacteria species and temperature

Abstract The immunocompetence handicap hypothesis (ICHH) postulates that testosterone supports the development of secondary sexual traits while simultaneously suppressing immune function, creating a trade‐off between trait quality and pathogen vulnerability. The nature of interactions between testosterone and immunity is complex. Conflicting patterns from the literature suggest that testosterone–immunity relationships are variable across immune measures and may be modified by factors both intrinsic and extrinsic to the organism. In this study, we tested the ICHH in free‐ranging American alligators Alligator mississippiensis and examined how both intrinsic (steroid hormone levels) and extrinsic (temperature) factors modulate the relationship between testosterone and immunity. Specifically, we quantified the simultaneous effects of testosterone and dehydroepiandrosterone (DHEA) on microbial killing capacity of three bacteria species (Escherichia coli, Salmonella typhimurium and Klebsiella pneumoniae) at two challenge temperatures (15°C and 30°C). We found that accounting for circulating levels of DHEA was important for predicting testosterone‐mediated effects on microbial killing capacity. We also found that testosterone‐mediated immunosuppression was dependent on temperature and bacteria species, with negative effects of testosterone present only for S. typhimurium at 15°C. Our results highlight the context dependency of interactions between testosterone and immunity, and illustrate the importance of evaluating the ICHH in natural systems to identify key intrinsic and extrinsic factors modulating testosterone‐immunity trade‐offs. A free Plain Language Summary can be found within the Supporting Information of this article.

Steroid hormones, ectoparasites, and color: Sex, species, and seasonal differences in Sceloporus lizards

Testosterone, in addition to promoting the expression of sexual ornaments can negatively affect immune function, leaving individuals more susceptible to parasites (immunocompetence handicap hypothesis). Immunosuppressive effects of testosterone also can occur indirectly, through increased glucocorticoid hormones (corticosterone, cortisol). Therefore, the expression of sexual ornaments and the ability to respond to parasites and diseases may be influenced by the interaction between testosterone and corticosterone. In this study we examined correlations of both testosterone and corticosterone with ectoparasite load and with expression of colorful sexual ornaments (patches on belly and throat) in three species of Sceloporus lizards (S. grammicus, S. megalepidurus, S. torquatus). In addition, we evaluated contributions of sex, body condition, and reproductive season. We expected that individuals with higher testosterone and lower corticosterone levels would have more colorful ornaments than individuals with higher corticosterone levels. In addition, if testosterone has negative effects on immune function but only at higher corticosterone levels, individuals with higher levels of testosterone and corticosterone should have higher ectoparasite loads. Contrary to these expectations, we did not detect an interaction between testosterone and corticosterone statistically affecting either ectoparasite load or the expression of colorful ornaments. Further, we did not find a positive association of either testosterone or corticosterone on ectoparasite loads in any of the three study species. Only in S. grammicus males was a hormone statistically associated with ectoparasite load, but it was a negative association with testosterone. The relationships between both hormones and different aspects of the colorful patches (brightness and chroma) varied drastically among the three species as well as between sexes. Hence, even among congeneric species, we did not observe consistent patterns among color, steroid hormones and ectoparasites. Different associations between these variables may reflect different physiological strategies for the production of colorful signals and immune defense.

Sex-biased parasitism and expression of a sexual signal

AbstractGiven that sexual signals are often expressed more highly in one sex than the other, they can impose a sex-specific cost of reproduction through parasitism. The two primary paradigms regarding the relationship of parasites to sexual signals are the good genes hypothesis and the immunocompetence handicap hypothesis; however, there are other ecological, morphological and energetic factors that might influence parasite infections in a sex-specific fashion. We tested the relationship between expression of a sexual signal (the dewlap) and ecological, morphological and energetic factors mediating ectoparasite (mite) load between male and female Panamanian slender anoles (Anolis apletophallus). We found that males were more highly parasitized than females because of the preponderance of ectoparasites on the larger dewlap of males. Indeed, ectoparasite infection increased with both body size and dewlap size in males but not in females, and parasite infection was related to energy storage in a sex-specific fashion for the fat bodies, liver and gonads. Our work and previous work on testosterone in anoles suggests that this pattern did not arise solely from immunosuppression by testosterone, but that mites prefer the dewlap as an attachment site. Thus, the expression of this sexual signal could incur a fitness cost that might structure life-history trade-offs.

Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

Sexually selected traits are hypothesized to be honest signals of individual quality due to the costs associated with their maintenance, development, and/or production. Testosterone, a sex steroid associated with the development and/or production of sexually selected traits, has been proposed to enforce the honesty of sexually selected traits via its immunosuppressive effects (i.e., the Immunocompetence Handicap Hypothesis) and/or by influencing an individual’s exposure/susceptibility to oxidative stress (i.e., the Oxidation Handicap Hypothesis). Previous work testing these hypotheses has primarily focused on physiological measurements of immunity or oxidative stress, but little is known about the molecular pathways by which testosterone could influence immunity and/or oxidative stress pathways. To further understand the transcriptomic consequences of experimentally elevated testosterone in the context of handicap hypotheses, we used previously published RNA-seq data from studies that measured the transcriptome of individuals treated with either a testosterone-filled or an empty (i.e., control) implant. Two studies encompassing three species of bird and three tissue types fit our selection criteria and we reanalyzed the data using weighted gene co-expression network analysis. Testosterone-treated individuals exhibited signatures of immunosuppression and our results describe the molecular pathways underlying this effect. We also provide some evidence to suggest that the transcriptomic signature of immunosuppression is evolutionarily conserved between the three species. While our results provide no evidence to suggest testosterone mediates handicaps via pathways associated with oxidative stress, they do support the hypothesis that testosterone enforces the honesty of sexually-selected traits by influencing an individual’s immunocompetence. Overall, this study develops a framework for testing testosterone-mediated handicap hypotheses and provides guidelines for future integrative and comparative studies focused on the proximate mechanisms mediating sexually selected traits.

Immune function during early adolescence positively predicts adult facial sexual dimorphism in both men and women

Evolutionary theories suggest that humans prefer sexual dimorphism in faces because masculinity in men and femininity in women may be an indicator of immune function during development. In particular, the immunocompetence handicap hypothesis proposes that sexual dimorphism indicates good immune function during development because the sex hormones, particularly testosterone in men, required for the development of sexually dimorphic facial features also taxes the immune system. Therefore, only healthy males can afford the high level of testosterone for the development of sexually dimorphic traits without compromising their survival. Researchers have suggested that a similar mechanism via the effects of oestrogen might also explain male preferences for female femininity. Despite the prominence of the immunocompetence handicap hypothesis, no studies have tested whether immune function during development predicts adult facial sexual dimorphism. Here, using data from a longitudinal public health dataset, the Western Australian Pregnancy Cohort (Raine) Study (Generation 2), we show that some aspects of immune function during early adolescence (14 years) positively predict sexually dimorphic 3D face shape in both men and women. Our results support a fundamental assumption that facial sexual dimorphism is an indicator of immune function during the development of facial sexual dimorphism.

Testosterone is positively and estradiol negatively associated with mucosal immunity in Amazonian adolescents.

A core assumption of life history theory and the immunocompetence handicap hypothesis (ICHH) is that testosterone (T) upregulates energetic investment in mating effort at the expense of immunity. This tenet, along with observed positive relationships between estrogens and immunity, may contribute to the higher observed morbidity and mortality of males. In the present study, we examine the association between sex steroid hormones and mucosal immunity as well as sex differences in immunity in a rural Amazonian population of immune-challenged Bolivian adolescents. Salivary steroid hormones (T [males only] and estradiol [E2 , females only]), Tsimane-specific age-standardized BMI z-scores, and salivary mucosal immunity (sIgA, secretory IgA) were measured in 89 adolescent males and females. Males had significantly higher sIgA levels than females, which may be due to the observed immune-endocrine associations found in the present study. Controlling for age and phenotypic condition, higher T significantly predicted higher sIgA; whereas higher E2 was associated with lower sIgA in females. Results stood in contrast to common interpretations of the ICHH, that is, that T should be inversely associated with immunity. Findings from the present study support the notion that the endocrine system likely affects immunity in a regulatory fashion, upregulating certain aspects of immunity while downregulating others. An important remaining question is the adaptive reason(s) for sex differences in endocrine-mediated immuno-redistribution.

Social and endocrine correlates of immune function in meerkats: implications for the immunocompetence handicap hypothesis.

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a female-dominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual's sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males.

Do men with more masculine voices have better immunocompetence?

Abstract The human voice is often considered to be a secondary sexual characteristic that signals underlying information about the immunocompetence of the speaker (i.e. the immunocompetence handicap hypothesis; ICHH). However, no studies have yet shown a relationship between vocal characteristics and biomarkers of immune function or self-reported health. In a sample of 108 men, we examined correlations between masculine vocal characteristics [i.e. relatively low fundamental frequency (F0), low F0 variability (F0-SD), low formant position (Pf), and high vocal tract length (VTL)] in relation to salivary immunoglobulin-A (sIgA; a marker of mucosal immunity), testosterone (T), and well-validated measures of self-reported health status. Results showed that sIgA correlated with masculinized F0, Pf, and VTL. Self-report health correlated with masculinized Pf and VTL. Anticipated future health correlated negatively with F0-SD and sick role propensity (less interference of illness in daily life) correlated positively with VTL. Perceived susceptibility to infection correlated with more feminized F0 and F0-SD. Our results demonstrated a small relationship between men's vocal characteristics and one putative indicator of mucosal immunity along with self-identified health status. We suggest that more research is warranted to determine whether the masculinity of men's voices may serve as an indicator of their phenotypic quality.

No evidence for the immunocompetence handicap hypothesis in male humans

The observations that testosterone might be immunosuppressive, form the basis for the immunocompetence handicap hypothesis (ICHH). According to ICHH only high-quality individuals can maintain high levels of testosterone and afford the physiological cost of hormone-derived immunosuppression. The animal and human studies that attempted to support the ICHH by precisely defined impairment of immunity associated with high testosterone levels are inconclusive. Furthermore, human studies have used only selected immune functions and varying testosterone fractions. This is the first study examining the relationship between multiple innate and adaptive immunity and serum levels of free testosterone, total testosterone, DHT and DHEA in ninety-seven healthy men. Free testosterone and marginally DHT levels were positively correlated with the strength of the influenza post-vaccination response. Total testosterone and DHEA showed no immunomodulatory properties. Our findings did not support ICHH assumptions about immunosuppressive function of androgens. In the affluent society studied here, men with higher levels of free testosterone could afford to invest more in adaptive immunity. Since the hormone-immune relationship is complex and may depend on multiple factors, including access to food resources, androgens should be treated as immunomodulators rather than implicit immunosuppressants.

A test of the effects of androgens on immunity: No relationship between 11-ketotestosterone and immune performance in bluegill (Lepomis macrochirus)

The immunosuppressive effects of androgens are a key component of the immunocompetence handicap hypothesis (ICHH). Here, we use bluegill sunfish (Lepomis macrochirus) to test two predictions arising from this hypothesis: (1) natural circulating concentrations of the androgen 11-ketotestosterone (11-KT) will be negatively related with measures of immunity, and (2) immune stimulation will lower circulating 11-KT concentration. We found no evidence for a relationship between natural circulating 11-KT concentration and measures of immunity (lymphocyte and granulocyte counts, respiratory burst, cytokine mRNA levels), and an immune stimulation with Vibrio vaccine did not affect circulating 11-KT concentration. We also performed a meta-analysis of immune stimulation studies to help interpret our results, and report evidence suggesting that immune stimulation has weaker effects on androgen levels in fishes compared to other vertebrates. These results suggest that the ICHH may not apply to all vertebrates, although it remains premature to state what factors account for the weaker evidence in fishes that androgens are immunosuppressive.

Trade-offs between immunity and testosterone in male African ground squirrels.

The immunocompetence handicap hypothesis (ICHH) proposes that testosterone has both beneficial effects on male reproductive potential and negative effects by suppressing the immune system. However, support for the ICHH has been variable and an alternative hypothesis suggests that testosterone may be acting indirectly via cortisol to suppress immunity (the stress-linked ICHH). A third hypothesis is that increased energetic investment in immunity results in the suppression of testosterone. We tested these hypotheses in male Cape ground squirrels (Xerus inauris) through two separate manipulations: first, by triggering a strong immune response using a lipopolysaccharide (LPS) injection and, secondly, by increasing circulating testosterone using silastic testosterone implants. Responding to an immune challenge significantly reduced testosterone, supporting the immune suppression hypothesis, while increasing circulating testosterone had no effect on immunocompetence, body mass, ectoparasite abundances or cortisol levels, failing to support either the ICHH or stress-linked ICHH. Our results add to the increasing body of literature that challenges the ICHH, and we conclude that the trade-off between testosterone and immunity is mediated through immune activation and not through testosterone in male Cape ground squirrels. Being able to test the ICHH, stress-linked ICHH and immune suppression hypotheses in a free-ranging mammal gives us a unique opportunity to examine the mechanisms mediating this trade-off.

Facial appearance reveals immunity in African men

Facial appearance is thought to indicate immunity in humans, but very few studies have tested this relationship directly. The aim of this study was to test the relationship between direct measures of immunity, perceived facial health and attractiveness, and facial cues in African men. We show that men with a stronger cytokine response are considered significantly more attractive and healthy. Men with more masculine, heavier facial features (i.e. muscular appearance) have a significantly higher cytokine response and appear significantly healthier and more attractive, while men with a yellower, lighter, “carotenoid” skin colour, have a marginally higher immune response and are also considered significantly more healthy and attractive. In contrast, more symmetrical, skinnier looking men appeared more attractive and healthier, but did not have a stronger cytokine response. These findings also shed new light on the “androgen-mediated” traits proposed by the immunocompetence handicap hypothesis (ICHH) and we propose that facial muscularity serves as a better estimate of an “androgen-mediated” trait than facial masculinity. Finally, we build on previous evidence to show that men’s facial features do indeed reveal aspects of immunity, even better than more traditional measures of health, such as body mass index (BMI).