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It has been hypothesized that androgens respond to the social interactions as a way to adjust the behavior of individuals to the challenges of the social environment in an adaptive manner. Therefore, it is expected that transient changes in circulating androgen levels within physiological scope should impact the state of the brain network that regulates social behavior, which should translate into adaptive behavioral changes. Here, we examined the effect that a transient peak in androgen circulating levels, which mimics socially driven changes in androgen levels, has on the forebrain state, which harbors most nuclei of the social decision-making network. For this purpose, we successfully induced transient changes in circulating androgen levels in an African cichlid fish (Mozambique tilapia, Oreochromis mossambicus) commonly used as a model in behavioral neuroendocrinology by injecting 11-ketotestosterone or testosterone, and compared the forebrain transcriptome of these individuals to control fish injected with vehicle. Forebrain samples were collected 30 min and 60 min after injection and analyzed using RNAseq. Our results showed that a transient peak in 11-ketotestosterone drives more accentuated changes in forebrain transcriptome than testosterone, and that transcriptomic impact was greater at the 30 min than at the 60 min post-androgen administration. Several genes involved in the regulation of translation, steroid metabolism, ion channel membrane receptors, and genes involved in epigenetic mechanisms were differentially expressed after 11-ketotestosterone or testosterone injection. In summary, this study identified specific candidate genes that may regulate socially driven changes in behavioral flexibility mediated by androgens. Fundação para a Ciência e Tecnologia - FCT info:eu-repo/semantics/publishedVersion

Males of many species must allocate limited energy budgets between mating and parenting effort. The Challenge Hypothesis provides a framework for understanding these life-history trade-offs via the disparate roles of testosterone (T) in aggression, sexual behavior, and parenting. It predicts that males pursuing mating opportunities have higher T than males pursuing paternal strategies, and in humans, many studies indeed report that men who are fathers and/or pair-bonded have lower T than childless and/or unpaired men. However, the magnitude of these effects, and the influence of methodological variation on effect sizes, have not been quantitatively assessed. We meta-analyzed 114 effects from 66 published and unpublished studies covering four predictions inspired by the Challenge Hypothesis. We confirm that pair-bonded men have lower T than single men, and fathers have lower T than childless men. Furthermore, men more oriented toward pair-bonding or offspring investment had lower T. We discuss the practical meaningfulness of the effect sizes we estimate in relation to known factors (e.g., aging, geographic population) that influence men’s T concentrations.

Testosterone (T) is a sexual hormone capable of modulating several traits in birds, including aggressiveness and reproductive behavior. Although variation in T-related traits is well-known for temperate zone birds, this variation has not been extensively studied in tropical species. The campo miner (Geositta poeciloptera) is a threatened bird endemic to the grasslands of the South American Cerrado. We investigated the seasonal variation in plasma T levels and associated behavior in the campo miner, addressing the following questions: (1) Does the species exhibit seasonal variation in T profile? (2) Do males have higher plasma T levels than females, irrespective of season? (3) Are males with higher plasma T levels more aggressive than males with lower T levels? (4) Do males' plasma T levels decrease after females lay eggs? We found that T levels are higher during the breeding season than during the nonbreeding season and that males present higher T levels than females throughout the year. Such high T levels are associated with a higher probability to engage in aggressive behavior; however, T levels decline toward the egg-laying date and keep decreasing afterward. Higher T levels before egg laying are apparently related to territorial defense against invaders and extrapair copulations. With the beginning of parental care, T levels decrease, which is in line with previous observations that the species becomes less aggressive after egg laying. This study contributes to the understanding of environmental endocrinology of tropical birds, filling some knowledge gaps about the diverse Neotropical avifauna.

Our understanding of the proximate and ultimate mechanisms shaping competitive reproductive phenotypes primarily stems from research on male-male competition for mates, even though competition is widespread in both sexes. We evaluate the hypothesis that the restricted nature of a resource required for reproduction, i.e. nest site, is a key variable driving territorial competition and testosterone secretion in female and male birds. Obligate secondary cavity-nesting has evolved repeatedly across avian lineages, providing a useful comparative context to explore how competition over limited nest cavities shapes aggression and its underlying mechanisms across species. Although evidence from one or another cavity-nesting species suggests that territorial aggression is adaptive in both females and males, this has not yet been tested in a comparative framework. We predicted that cavity-nesting generates more robust territorial aggression, in comparison to close relatives with less restrictive nesting strategies. Our focal species were two obligate secondary cavity-nesting species and two related species with more flexible nesting strategies in the same avian family: tree swallow (Tachycineta bicolor) vs. barn swallow (Hirundo rustica); Eastern bluebird (Sialia sialis) vs. American robin (Turdus migratorius). We assayed conspecific aggression using simulated territorial intrusion and found that cavity-nesting species displayed greater territorial aggression than their close relatives. This pattern held for both females and males. Because territorial aggression is often associated with elevated testosterone, we also hypothesized that cavity-nesting species would exhibit higher testosterone levels in circulation. However, cavity-nesting species did not have higher testosterone in circulation for either sex, despite some correlative evidence that testosterone is associated with higher rates of physical attack in female tree swallows. Our focus on a context that is relevant to both sexes - competition over essential breeding resources - provides a useful framework for co-consideration of proximate and ultimate drivers of reproductive competition in females and males.

Territorial behaviour has been widely described across many animal taxa, where the acquisition and defence of a territory are critical for the fitness of an individual. Extensive evidence suggests that androgens (e.g. testosterone) are involved in the modulation of territorial behaviour in male vertebrates. Short-term increase of androgen following a territorial encounter appears to favour the outcome of a challenge. The “Challenge Hypothesis” proposed by Wingfield and colleagues outlines the existence of a positive feedback relationship between androgen and social challenges (e.g. territorial intrusions) in male vertebrates. Here we tested the challenge hypothesis in the highly territorial poison frog, Allobates femoralis, in its natural habitat by exposing males to simulated territorial intrusions in form of acoustic playbacks. We quantified repeatedly androgen concentrations of individual males via a non-invasive water-borne sampling approach. Our results show that A. femoralis males exhibited a positive behavioural and androgenic response after being confronted to simulated territorial intrusions, providing support for the Challenge Hypothesis in a territorial frog.

Testosterone is often considered a critical regulator of aggressive behaviour. There is castration/replacement evidence that testosterone indeed drives aggression in some species, but causal evidence in humans is generally lacking and/or—for the few studies that have pharmacologically manipulated testosterone concentrations—inconsistent. More often researchers have examined differences in baseline testosterone concentrations between groups known to differ in aggressiveness (e.g., violent vs non-violent criminals) or within a given sample using a correlational approach. Nevertheless, testosterone is not static but instead fluctuates in response to cues of challenge in the environment, and these challenge-induced fluctuations may more strongly regulate situation-specific aggressive behaviour. Here, we quantitatively summarize literature from all three approaches (baseline, change, and manipulation), providing the most comprehensive meta-analysis of these testosterone-aggression associations/effects in humans to date. Baseline testosterone shared a weak but significant association with aggression (r = 0.054, 95% CIs [0.028, 0.080]), an effect that was stronger and significant in men (r = 0.071, 95% CIs [0.041, 0.101]), but not women (r = 0.002, 95% CIs [−0.041, 0.044]). Changes in T were positively correlated with aggression (r = 0.108, 95% CIs [0.041, 0.174]), an effect that was also stronger and significant in men (r = 0.162, 95% CIs [0.076, 0.246]), but not women (r = 0.010, 95% CIs [−0.090, 0.109]). The causal effects of testosterone on human aggression were weaker yet, and not statistically significant (r = 0.046, 95% CIs [−0.015, 0.108]). We discuss the multiple moderators identified here (e.g., offender status of samples, sex) and elsewhere that may explain these generally weak effects. We also offer suggestions regarding methodology and sample sizes to best capture these associations in future work.

The Challenge Hypothesis (Wingfield et al. Am. Nat. 136, 829-846) aims to explain the complex relationship between androgens and social interactions. Despite its well acceptance in the behavioral endocrinology literature, several studies have failed to found an androgen response to staged social interactions. Possible reasons for these inconsistencies are the use of single sampling points that may miss the response peak, and the occurrence of inter-individual variability in the androgen response to social interactions. In this study we addressed these two possible confounding factors by characterizing the temporal pattern of the androgen response to social interactions in the African cichlid, Oreochromis mossambicus, and relating it to inter-individual variation in terms of the individual scope for androgen response (i.e. the difference between baseline and maximum physiological levels for each fish) and behavioral types. We found that the androgen response to territorial intrusions varies between individuals and is related to their scope for response. Individuals that have a lower scope for androgen response did not increase androgens after a territorial intrusion but were more aggressive and exploratory. In contrast males with a higher scope for response had fewer aggressive and exploratory behaviors and exhibited two peaks of KT, an early response 2-15 min after the interaction and a late response at 60-90 min post-interaction. Given that the pharmacological challenge of the Hypothalamic-Pituitary-Gonad axis only elicits the late response, we suggest that these two peaks may be regulated by different physiological mechanisms, with the early response being mediated by direct brain-gonad neural pathways. In summary, we suggest that determining the temporal pattern of the androgen response to social interactions and considering inter-individual variation may be the key to understanding the contradictory results of the Challenge Hypothesis. Fundação para a Ciência e Tecnologia - FCT info:eu-repo/semantics/publishedVersion

Objectives This study examined potentially bidirectional connections of older U.S. women’s salivary testosterone with their social network connections. Methods Data were from the 2005–2006 and 2010–2011 waves of the National Social Life, Health and Aging Project (NSHAP), a national probability sample of older U.S. adults. Autoregressive cross-lagged panel models tested linkages of women’s testosterone with their social networks. Results Consistent with recent biological theory suggesting social modulation of hormones, a higher kin proportion in one’s egocentric (person-centered) network, arguably a stable compositional feature, negatively predicted women’s testosterone levels. In contrast, findings for tie strength were consistent with hormonal regulation of women’s sociality—with both perceived support from friends and family, and closeness to network members, negatively influenced by testosterone. Discussion Rather than being a static and exogenous biological factor, older women’s testosterone levels seem partly an outcome of their social context. Implications for sexual health and hormone therapy are discussed. However, this androgen also influences dimensions of their intimate networks critical to successful aging. Findings suggest the need for social scientists to engage with the neuroendocrine literature, which offers suggestions on linkages of hormones with specific network patterns.

Hormones can facilitate the expression of behavior, but relatively few studies have considered individual variation and repeatability in hormone-behavior relationships. Repeated measures of hormones are valuable because repeatability in hormone levels might be a mechanism that drives repeatability in behavior ("personality"). Testosterone is predicted to promote territorial aggression and suppress parental behaviors. In our population of eastern bluebirds (Sialia sialis), parental care and nest defense aggression toward a heterospecific are repeatable. We tested the hypothesis that repeatability of testosterone levels within individuals underlies repeatable behaviors observed in our population. We measured nestling provisioning and aggressive nest defense against a heterospecific. After behavioral observations we captured either the male or female bluebird, and determined initial testosterone levels and maximum capacity of the gonads to secrete testosterone by injecting gonadotropin-releasing hormone (GnRH). We found among-individual variation in initial testosterone levels for males and females. Individual males were repeatable in both initial and GnRH-induced testosterone levels across behavioral contexts, while individual females were repeatable in GnRH-induced testosterone levels. However, testosterone levels were not significantly related to parental or nest defense behaviors, suggesting that repeatable testosterone levels may not drive repeatable parental and heterospecific nest defense behaviors in this population. The absence of a relationship between testosterone and parental and heterospecific nest defense behaviors might be due to among-individual variation in testosterone levels. Considering the sources of variation in testosterone levels may reveal why some populations exhibit high individual variation in hormone levels.

Considerable evidence suggests that the steroid hormone testosterone mediates major life-history trade-offs in vertebrates, promoting mating effort at the expense of parenting effort or survival. Observations from a range of wild primates support the "Challenge Hypothesis," which posits that variation in male testosterone is more closely associated with aggressive mating competition than with reproductive physiology. In both seasonally and non-seasonally breeding species, males increase testosterone production primarily when competing for fecund females. In species where males compete to maintain long-term access to females, testosterone increases when males are threatened with losing access to females, rather than during mating periods. And when male status is linked to mating success, and dependent on aggression, high-ranking males normally maintain higher testosterone levels than subordinates, particularly when dominance hierarchies are unstable. Trade-offs between parenting effort and mating effort appear to be weak in most primates, because direct investment in the form of infant transport and provisioning is rare. Instead, infant protection is the primary form of paternal investment in the order. Testosterone does not inhibit this form of investment, which relies on male aggression. Testosterone has a wide range of effects in primates that plausibly function to support male competitive behavior. These include psychological effects related to dominance striving, analgesic effects, and effects on the development and maintenance of the armaments and adornments that males employ in mating competition.

The bi-directional links between hormones and behavior have been a rich area of research for decades. Theory on the evolution of testosterone (T) was greatly advanced by the challenge hypothesis, which presented a framework for understanding interspecific, seasonal, and social variation in T levels in males, and how they are shaped by the competing demands of parental care and male-male competition. Female competition is also widespread in nature, although it is less clear whether or how the challenge hypothesis applies to females. Here, we evaluate this issue in four parts: (1) We summarize and update prior analyses of seasonal plasticity and interspecific variation in T in females. (2) We evaluate experimental links between T and female aggression on shorter timescales, asking how T manipulations affect aggression and conversely, how social manipulations affect T levels in female mammals, birds, lizards, and fishes. (3) We examine alternative mechanisms that may link aggression to the social environment independently of T levels in circulation. (4) We present a case study, including new data analyses, in an aggressive female bird (the tree swallow, Tachycineta bicolor) to explore how variation in tissue-level processing of T may bridge the gap between circulating T and variation in behavior that is visible to natural selection. We close by connecting these multivariate levels of sex steroid signaling systems alongside different temporal scales (social, seasonal, and evolutionary) to generate broadly applicable insights into how animals respond to their social environment, regardless of whether they are male or female.

Almost fifty years ago the advent of assay methods to measure circulating levels of hormones revolutionized endocrinology in relation to investigations of free-living and captive animals. This new field "environmental endocrinology" revealed that endocrine profiles in animals in their natural habitat were not only different from captive animals, but often deviated from predictions. It quickly became apparent that the organization and analysis of data from the field should be sorted by life history stages such as for reproductive processes, migration, molt etc. and spaced in time according to natural duration of those processes. Presentation of data by calendar date alone gives much simpler, even misleading, patterns. Stage-organized analyses revealed species-specific patterns of hormone secretion and dramatic inter-individual differences. The "Challenge Hypothesis" sparked exploration of these results, which diverged from expectations of hormone-behavior interactions. The hypothesis led to specific predictions about how the hypothalamo-pituitary-gonad axis, and particularly circulating patterns of testosterone, might respond to social challenges such as simulated territorial intrusions. Initially, a group of studies on free-living and captive birds played a key role in the formulation of the hypothesis. Over the decades since, the effects of social challenge and environmental context on hormonal responses have been tested in all vertebrate taxa, including humans, as well as in insects. Although it is now clear that the Challenge Hypothesis in its original form is simplistic, field and laboratory tests of the hypothesis have led to other concepts that have become seminal to the development of environmental endocrinology as a field. In this special issue these developments are addressed and examples from many different taxa enrich the emerging concepts, paving the way for investigations using recent technologies for genetic and transcriptome analyses.

In this paper I discuss how the challenge hypothesis (Wingfield et al., 1990) influenced the development of ideas about animal personality, and describe particularly promising areas for future study at the intersection of these two topics. I argue that the challenge hypothesis influenced the study of animal personality in at least three specific ways. First, the challenge hypothesis drew attention to the ways in which the environment experienced by an organism - including the social environment - can influence biological processes internal to the organism, e.g. changes to physiology, gene expression, neuroendocrine state and epigenetic modifications. That is, the challenge hypothesis illustrated the bidirectional, dynamic relationship between hormones and (social) environments, thereby helping us to understand how behavioral variation among individuals can emerge over time. Because the paper was inspired by data collected on free living animals in natural populations, it drew behavioral ecologists' attention to this phenomenon. Second, the challenge hypothesis highlighted what became a paradigmatic example of a hormonal mechanism for a behavioral spillover, i.e. testosterone's pleiotropic effects on both territorial aggression and parental care causes aggression to "spillover" to influence parenting behavior, thereby limiting behavioral plasticity. Third, the challenge hypothesis contributed to what is now a cottage industry examining individual differences in hormone titres and their relationship with behavioral variation. I argue that one particularly promising future research direction in this area is to consider the active role of behavior and behavioral types in eliciting social interactions, including territorial challenges.

According to the Challenge Hypothesis, social interactions, particularly among males, have a strong influence on circulating androgen levels. Specifically, males should respond to social challenges from conspecific males with a rapid increase in plasma androgen levels which support and stimulate further aggression. This basic tenet of the Challenge Hypothesis, an androgen increase in response to a social challenge from another male, has been tested in all vertebrate classes. While early studies generally supported the Challenge Hypothesis, more recent work has noted numerous exceptions, particularly in birds. Here, we conduct a meta-analysis of studies in fish, amphibians, non-avian reptiles, and mammals that test the prediction that circulating androgen levels of males should increase in response to an experimental challenge from another male. We found that teleost fish often increase androgens during such challenges, but other vertebrate groups show more mixed results. Why should fish be different from the other taxa? In fish with paternal care of young, the potential conflict between mating, being aggressive towards other males, and taking care of offspring is alleviated, because females typically choose males based on their defense of an already existing nest. Hence, rather than regulating the trade-off between mating, aggression, and parenting, androgens may have been co-opted to promote all three behaviors. For other taxa, increasing androgen levels only makes sense when the increase directly enhances reproductive success. Thus, the increase in androgen levels is a response to mating opportunities rather than a response to challenge from another male. To further our understanding of the role of a change in androgen levels in mediating behavioral decision-making between mating, aggression, and parenting, we need studies that address the behavioral consequences of an increase in androgens after male-male encounters and studies that test the androgen responsiveness of species that differ in the degree of paternal care.

The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The hypothesis has been tested many times over the past 30years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.

Exhibiting behavioral plasticity in order to mount appropriate responses to dynamic and novel social environments is crucial to the survival of all animals. Thus, how animals regulate flexibility in the timing, duration, and intensity of specific behaviors is of great interest to biologists. In this review, we discuss how animals rapidly respond to social challenges, with a particular focus on aggression. We utilize a conceptual framework to understand the neural mechanisms of aggression that is grounded in Wingfield and colleagues' Challenge Hypothesis, which has profoundly influenced how scientists think about aggression and the mechanisms that allow animals to exhibit flexible responses to social instability. Because aggressive behavior is rooted in social interactions, we propose that mechanisms modulating prosocial behavior may be intricately tied to mechanisms of aggression. Therefore, in order to better understand how aggressive behavior is mediated, we draw on perspectives from social neuroscience and discuss how social context, species-typical behavioral phenotype, and neural systems commonly studied in relation to prosocial behavior (i.e., neuropeptides) contribute to organizing rapid responses to social challenges. Because complex behaviors are not the result of one mechanism or a single neural system, we consider how multiple neural systems important for prosocial and aggressive behavior (i.e., neuropeptides and neurosteroids) interact in the brain to produce behavior in a rapid, context-appropriate manner. Applying a systems neuroscience perspective and seeking to understand how multiple systems functionally integrate to rapidly modulate behavior holds great promise for expanding our knowledge of the mechanisms underlying social behavioral plasticity.

Several studies have shown that mothers and fathers have significant lower levels of testosterone (T) than non-mothers and non-fathers, and that in men caregiving is related to a decrease in T. To date, only a few studies have examined T in women. We examined T reactivity to a crying infant simulator in 160 women. Use of oral contraceptives (OC), basal cortisol (CORT) levels and childhood experiences of maternal love withdrawal were taken into account. T levels were consistently significantly higher in women not using OC. In women not using OC, high basal CORT was related to higher initial T levels and larger decreases of T during caregiving. No effect of basal CORT was found in women with OC use. Childhood experiences of maternal love withdrawal did not affect T levels. This is the first study to show support for a decrease of T in women while taking care of a crying infant, supporting the Challenge hypothesis and the Steroid/Peptide Theory of Social Bonds.

This study used population-representative longitudinal data from the 2005-2006 and 2010-2011 waves of the National Social Life, Health and Aging Project-a probability sample of US adults aged 57-85 at baseline (N = 650 women and 620 men)-to examine the causal direction in linkages of endogenous testosterone (T) with sexual activity and relationship quality. For both genders, our autoregressive effects indicated a large amount of temporal stability, not just in individual-level attributes (T, masturbation) but also dyadic ones (partnered sex, relationship quality)-indicating that a need for more nuanced theories of relational processes. Cross-lagged results suggested gender-specific effects-generally more consistent with sexual or relational modulation of T than with hormonal causation. Specifically, men's findings indicated their T might be elevated by their sexual (masturbatory) activity but not vice versa, although androgen levels did lower men's subsequent relationship quality. Women's T, in contrast, was negatively influenced not just by their higher relationship quality but also by their more frequent partnered sex-perhaps reflecting a changing function of sexual activity in late life.

Contains fulltext : 216742.pdf (Publisher’s version ) (Open Access) The Hypothalamus-Pituitary-Gonadal (HPG)-axis, and testosterone in particular, play an important role in social motivational behavior. Socially avoidant behavior, characteristic of social anxiety disorder (SAD), has been linked to low endogenous testosterone levels, and can be alleviated by testosterone administration in SAD. Although these beneficial effects of testosterone may translate to exposure therapy, it remains unknown whether testosterone increases prior to exposure improve therapy outcomes. In this proof-of-principle study, we tested whether pre-exposure (reactive and baseline) endogenous testosterone levels were predictive of exposure outcome in SAD. Seventy-three participants (52 females) with a principal SAD diagnosis performed four speech exposures: three during one standardized exposure therapy session and one at post-assessment one week later. Subjective fear levels were assessed before and after each speech exposure and social anxiety symptoms were assessed at pre- and post-treatment. Pre-treatment testosterone levels were assessed before (baseline) and in response to a pre-exposure instruction session (reactive). Pre-treatment testosterone levels were not related to fear levels during exposure therapy, but predicted pre- to post-treatment reductions in social anxiety symptom severity. Specifically, low baseline and high reactive pre-treatment testosterone levels were associated with larger reductions in social anxiety symptom severity. These findings support the role of HPG-axis in social fear reduction. Specifically, our finding that high reactive testosterone as well as low baseline testosterone predicted exposure outcome in SAD, suggests that good reactivity of the HPG-axis is a promising marker for the symptom-reducing effects of exposure therapy. 6 p.

For most cetacean species, there is little known about how an individual's physiology influences its behaviour. Humpback whales (Megaptera novaeangliae) are a good candidate to examine such links as they have a well-described distribution and behaviour, can be consistently sampled using remote biopsy systems, and have been the subject of several previous endocrine studies. The objective here was to examine whether a female humpback whale's social state (i.e. escorted by a male or not) is related to her endocrine condition, and whether male dominance ranking is related to testosterone levels. Skin and blubber biopsies were collected from the east and west Australian humpback whale populations in 2010–2016 (n = 252) at multiple times throughout the winter-spring breeding season. Steroid hormones were extracted from blubber and concentrations of progesterone (a marker for pregnancy), testosterone (a marker of male testicular activity) and oestradiol (a potential marker of ovarian activity) measured using enzyme-immunoassays. Principal escorts—the dominant males in mixed sex groups—had significantly higher blubber testosterone levels (mean ± SE; 1.43 ± 0.20 ng/g wet weight) than subordinate, secondary escorts (0.69 ± 0.06 ng/g wet weight). Females that were escorted by males typically possessed elevated blubber oestradiol levels (1.96 ± 0.25 ng/g wet weight; p = 0.014); few were considered to be pregnant (p = 0.083). ‘Unescorted’ females displayed characteristically lower blubber oestradiol levels (0.56 ± 0.06 ng/g wet weight). Together, these results are consistent with ‘challenge hypothesis’ theory and suggest the existence of associated reproductive patterns in humpback whales.

Objective Cross-culturally, men's T declines in response to pairbonding and fatherhood, but less is known about what happens to T during and after life history transitions that theoretically lead to renewed mating effort. We tested whether men's T rises (or declines less with age) as their children age, or when pairbonds end, independent of changes in fatherhood-related variables such as co-residence with children. Methods We used demographic, behavioral, and salivary hormone data (waking and pre-bed T) collected in 2009 and 2014 for the Cebu Longitudinal Health and Nutrition Survey (n = 571 men). Results Fathers with older children tended to have attenuated decline in pre-bedtime T between 2009 and 2014 compared to men with younger children, after controlling for pairbonding (s = 1.58, SE = 0.88, P = 0.074). Separated men had higher pre-bedtime T than pairbonded men, controlling for fatherhood-related variables (s = 11.74, SE = 4.33, P = 0.007). Change in T did not significantly differ for men who separated between the two surveys, relative to men who remained pairbonded throughout. Conclusion We found modest support for the prediction that men experience less of an age-related drop in T as their youngest child ages, a trend that might strengthen as children age further. We also replicate the finding that separated men have higher T, although longitudinal changes in the hormone were not significantly different in these men. Our data suggest that, of two life history transitions that may predict renewed mating effort, pair bond loss is more strongly endocrine mediated than potential mating effort shifts related to the aging of children.

In this study, we describe an approach based on an individual's hormonal reactive scope to study short-term effects of hormones on behavior. The control of territorial aggression has been traditionally linked to testosterone. Males of some vertebrate species show an increase in testosterone during territorial interactions and implantation studies suggest that such an increase in testosterone enhances the intensity and persistence of aggression. Here, we tested whether a short-term maximum release of testosterone – based on an individual's hormonal reactive scope – affects the intensity or persistence of territorial aggression in male black redstarts, a bird species in which testosterone does not increase during territorial encounters. An injection with gonadotropin-releasing-hormone (GnRH) induced a physiological peak in plasma testosterone that was specific for each individual (= individual reactive scope). However, such short-term surges in an individual's testosterone concentration did not affect the intensity or persistence of aggression. In conclusion, this study demonstrated (1) that a species that naturally does not increase testosterone during male–male encounters would not benefit from such an increase in terms of being more aggressive, (2) that behavioral studies using GnRH-injections represent a promising approach to study species differences in androgen responsiveness, and (3) that injections of releasing or tropic hormones in general may be a suitable approach to study short-term influences of hormones on behavior. These injections effectively mimic the potential short-term changes in hormones that can occur in the real life of individuals and enable us to study the effects of hormonal changes on behavior or other traits within an ecological and evolutionary framework.

This study evaluated the effect of game venue and starting status on precompetitive psychophysiological measures in elite rugby union. Saliva samples were taken from players (starting XV, n = 15, and nonstarters, n = 9) on a control day and 90 min before 4 games played consecutively at home and away venues against local rivals and league leaders. Precompetition psychological states were assessed using the Competitive State Anxiety Inventory−2. The squad recorded 2 wins (home) and 2 losses (away) over the study period. Calculated effect sizes (ESs) showed higher pregame cortisol- (C) and testosterone- (T) difference values before all games than on a baseline control day (ES 0.7−1.5). Similar findings were observed for cognitive and somatic anxiety. Small between-venues C differences were observed in starting XV players (ES 0.2−0.25). Conversely, lower home T- (ES 0.95) and higher away C- (ES 0.6) difference values were observed in nonstarters. Lower T-difference values were apparent in nonstarters (vs starting XV) before home games, providing evidence of a between-groups effect (ES 0.92). Findings show an anticipatory rise in psychophysiological variables before competition. Knowledge of starting status appears a moderating factor in the magnitude of player endocrine response between home and away games.

© 2016 A contribution to a special issue on Hormones and Human Competition. The relationship between androgenic hormones, like testosterone (T), and aggression is extensively studied in human populations. Yet, while this work has illuminated a variety of principals regarding the behavioral and phenotypic effects of T, it is also hindered by inherent limitations of performing research on people. In these instances, animal research can be used to gain further insight into the complex mechanisms by which T influences aggression. Here, we explore recent studies on T and aggression in numerous vertebrate species, although we focus primarily on males and on a New World rodent called the California mouse (Peromyscus californicus). This species is highly territorial and monogamous, resembling the modern human social disposition. We review (i) how baseline and dynamic T levels predict and/or impact aggressive behavior and disposition; (ii) how factors related to social and physical context influence T and aggression; (iii) the reinforcing or “rewarding” aspects of aggressive behavior; and (iv) the function of T on aggression before and during a combative encounter. Included are areas that may need further research. We argue that animal studies investigating these topics fill in gaps to help paint a more complete picture of how androgenic steroids drive the output of aggressive behavior in all animals, including humans.

Urban songbirds of several species more vigorously defend their territories in response to conspecific song playback than do their rural counterparts, but the hormonal basis of this behavioral difference is unclear. It is well established in vertebrates that both testosterone and corticosterone affect the intensity of territoriality. Previous studies have found no evidence that initial (i.e., immediately following territorial challenge, but prior to restraint) plasma testosterone accounts for the elevated territorial aggression of urban birds. Determining if testosterone still contributes to urban-rural differences in territoriality requires also assessing males' abilities to transiently increase plasma testosterone (in response to an injection of gonadotropin-releasing hormone). We tested whether these hormones are correlated with the territorial response to conspecific song playback in urban and rural male Song Sparrows (Melospiza melodia) in Montgomery County, Virginia. We found that the elevated territorial aggression of urban sparrows was not related to variation in either initial plasma testosterone or the ability to transiently increase testosterone. In contrast, despite no overall habitat difference in initial corticosterone, levels of this hormone were positively correlated with territoriality in urban and rural sparrows. Furthermore, for a given level of corticosterone, urban sparrows were more territorially aggressive. Our findings suggest that initial corticosterone may either play a role in the regulation of persistent differences in territorial behavior between free-ranging urban and rural male Song Sparrows or be affected by the intensity of behavioral response to territorial challenge.

The Challenge Hypothesis, designed originally to explain the patterning of competitive behavior and androgen levels in seasonally breeding birds, predicts that males will increase their androgen levels in order to become more competitive in reproductive contexts. Here we test predictions derived from the Challenge Hypothesis in white-faced capuchin monkeys (Cebus capucinus), a species that has somewhat seasonal reproduction. We analyzed demographic and hormonal data collected over a 5.25-year period, from 18 males in nine social groups living in or near Lomas Barbudal Biological Reserve, Costa Rica. Alpha males had higher androgen levels than subordinates. Contrary to our predictions, neither the number of breeding-age males nor the number of potentially fertile females was obviously associated with androgen levels. Furthermore, male androgen levels were not significantly linked to social stability, as measured by stability of male group membership or recency of change in the alpha male position. Androgen levels changed seasonally, but not in a manner that had an obvious relationship to predictions from the Challenge Hypothesis: levels were generally at their lowest near the beginning of the conception season, but instead of peaking when reproductive opportunities were greatest, they were at their highest near the end of the conception season or shortly thereafter. This lack of correspondence to the timing of conceptions suggests that there may be ecological factors not yet identified that influence ifA levels. We expected that the presence of offspring who were young enough to be vulnerable to infanticide during an alpha male takeover might influence androgen levels, at least in the alpha male, but this variable did not significantly impact results.

The study of testosterone and aggression originated in experimental studies of animals, showing a direct causal link in some species. Human studies showed an overall weak correlation between testosterone and aggression. A theoretical framework ('the challenge hypothesis') enabled testosterone-behavior interactions in humans to be framed within a theory that emphasized hormonal responses to competition influencing subsequent aggressive behavior. The short-term administrations of testosterone to young women and to young men showed influences on behavioral and neural processes associated with aggression. Other findings are that testosterone influences aggression in high dominance men, and in those with low cortisol levels; and that testosterone can affect both aggressive and prosocial behavior, within the context of an experimental game.

Investigating causes and consequences of variation in hormonal expression is a key focus in behavioral ecology. Many studies have explored patterns of secretion of the androgen testosterone in male vertebrates, using the challenge hypothesis (Wingfield, Hegner, Dufty, & Ball, 1990; The American Naturalist, 136(6), 829–846) as a theoretical framework. Rather than the classic association of testosterone with male sexual behavior, this hypothesis predicts that high levels of testosterone are associated with male–male reproductive competition but also inhibit paternal care. The hypothesis was originally developed for birds, and subsequently tested in other vertebrate taxa, including primates. Such studies have explored the link between testosterone and reproductive aggression as well as other measures of mating competition, or between testosterone and aspects of male behavior related to the presence of infants. Very few studies have simultaneously investigated the links between testosterone and male aggression, other aspects of mating competition and infant‐related behavior. We tested predictions derived from the challenge hypothesis in wild male Barbary macaques (Macaca sylvanus), a species with marked breeding seasonality and high levels of male‐infant affiliation, providing a powerful test of this theoretical framework. Over 11 months, 251 hr of behavioral observations and 296 fecal samples were collected from seven adult males in the Middle Atlas Mountains, Morocco. Fecal androgen levels rose before the onset of the mating season, during a period of rank instability, and were positively related to group mating activity across the mating season. Androgen levels were unrelated to rates of male–male aggression in any period, but higher ranked males had higher levels in both the mating season and in the period of rank instability. Lower androgen levels were associated with increased rates of male‐infant grooming during the mating and unstable periods. Our results generally support the challenge hypothesis and highlight the importance of considering individual species’ behavioral ecology when testing this framework.

Testosterone levels show large variations over time and among individuals. Testosterone levels are determined by three factors: the physiological baseline, cyclical (often seasonal) reproductive patterns, and responses to social environment or challenges. Understanding the regulation of testosterone in this manner helps to explain its highly variable expression.

Testosterone and cortisol are hormones expected to play a major role in competitive behaviours (i.e. aggression), and are related to rank and hierarchical stability. Through a non-invasive technique, we analyzed faecal testosterone (FTM 1 ) and cortisol (FCM 2 ) metabolites of dominant and subordinate males from two wild groups of bearded capuchin monkeys. One group had a stable dominance hierarchy while the other had an unstable hierarchy, with a marked conflict period related to a male take-over. In the unstable hierarchy group (1) the dominant male had higher FTM peaks than subordinates, and (2) basal FTM levels were higher than in the stable group. These findings are in accordance with the Challenge Hypothesis and rank-based predictions, and confirm that in Sapajus libidinosus hierarchy stability, social status, aggression rates and testosterone are closely related. Dominants of both groups had higher basal and peak FCM levels, suggesting that in S. libidinosus the dominant male has a higher allostatic load than subordinates, related to his role in protection against predators, intragroup appeasement, and control of food sources. Finally, we suggest that males of S. libidinosus are resistant to testosterone suppression by cortisol, because in the unstable group in spite of an increase in FCM there was also an increase in FTM during the conflict period. This article is part of a Special Issue entitled: Neotropical Behaviour.

The challenge hypothesis posits a correlation between male androgen levels and mating system, male–male aggression in a sexual context, and parental effort. This model has received support across a variety of taxa, including primates. Most primate studies have focused on multi-male societies characterized by relatively high levels of male–male aggression and limited paternal care. To expand this dataset, predictions of the challenge hypothesis were tested in a population of wild siamangs (Symphalangus syndactylus), small apes characterized by intense territoriality, monogamous/polyandrous grouping patterns, and varying amounts of paternal behavior. Behavioral data were collected on 11 study groups (five two-male groups and six one-male groups). Seven hundred thirty-four fecal samples were collected from 18 adult males to quantify concentrations of fecal immunoreactive androgens (fiA) by radioimmunoassay. As predicted by the challenge hypothesis, males involved in the aggressive replacement of a resident male had significantly higher fiA concentrations than control males, while males displaying active parental care had significantly lower fiA concentrations than average. Results showed no association between male androgen concentration and group composition, male rank, or rate of intragroup male–male aggression. These latter findings, seemingly inconsistent with the hypothesis, could be explained by the clear and stable dominance relationships between co-resident males: given the very low rates of physical aggression, a low baseline testosterone is to be expected. Furthermore, the effects of increased intragroup conflict experienced by males in two-male groups might be offset by the higher frequency of intergroup aggression experienced by males in one-male groups.

Male courtship signals often stimulate the production of sex steroids in both female and male receivers. Such effects benefit signallers by increasing receptivity in females, but impose costs on signallers by promoting sexual behaviour and aggression in male competitors. To resolve this androgen-based conflict, males should use strategies that suppress sex steroid production in rival males. In green treefrogs, Hyla cinerea, chorus sounds (i.e. advertisement calls from aggregates of males) are known to stimulate androgen production in receiver males. Here, I examined whether males of this species counter these effects by eliciting an endocrine stress response in male conspecifics during close-range vocal interactions. I show that corticosterone (CORT) levels were higher in males that lost vocal contests in natural choruses compared to contest winners and nonaggressive males. Testosterone levels were also lower in contest losers compared to nonaggressive males, but not contest winners; dihydrotesterone levels did not differ among the three groups. Aggressive and advertisement calls were then broadcast to males in an experiment that simulated close-range vocal communication. Aggressive calls rapidly (45 min) elicited an increase in CORT and a reduction in androgens in receivers. Advertisement calls did not elicit an increase in CORT, but CORT levels were sustained relative to controls exposed to silence and were accompanied by a reduction in androgens in small males. Endocrine responses to acoustic signals in this species thus vary depending upon context, call type and size of signal receivers. Signallers benefit from eliciting CORT production in competitors because elevated CORT suppresses vocalization.

Photoperiod is a major environmental cue that signals breeding conditions in animals living in temperate climates. Therefore, the activity of the reproductive (i.e. hypothalamic–pituitary–gonadal, HPG) axis and of the expression of reproductive behaviors, including territoriality, is responsive to changes in day length. However, at low latitudes the seasonal variation in day length decreases dramatically and photoperiod becomes less reliable as a breeding entraining cue in tropical species. In spite of this, some tropical mammals and birds have been found to still respond to small amplitude changes in photoperiod (e.g. 17 min). Here we tested the effect of 2 photoperiod regimes, referred to as long-day (LD: 16L:08D) and short-day (SD: 08L:16D), on the activity of the HPG axis, on aggressive behavior and in the androgen response to social challenges in males of the tropical cichlid fish Tilapia rendalli. For each treatment, fish were transferred from a pre-treatment photoperiod of 12L:12D to their treatment photoperiod (either LD or SD) in which they were kept for 20 days on stock tanks. Afterwards, males were isolated for 4 days in glass aquaria in order to establish territories and initial androgen levels (testosterone, T; 11-ketotestosterone, KT) were assessed. On the 4th day, territorial intrusions were promoted such that 1/3 of the isolated males acted as residents and another 1/3 as intruders. Territorial intrusions lasted for 1 h to test the effects of a social challenge under different photoperiod regimes. Photoperiod treatment (either SD or LD) failed to induce significant changes in the HPG activity, as measured by androgen levels and gonadosomatic index. However, SD increased the intensity of aggressive behaviors and shortened the time to settle a dominance hierarchy in an androgen-independent manner. The androgen responsiveness to the simulated territorial intrusion was only present in KT but not for T. The percent change in KT levels in response to the social challenge was different between treatments (SD > LD) and between male types (resident > intruder). The higher androgen response to a social challenge in residents under SD may be explained by the time course of the androgen response that due to the long time it takes to fight resolution under LD, might have been delayed. This result illustrates the importance of incorporating time response data in social endocrinology studies. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil, PDSE fellowship; Fundação de Amparo à Pesquisa no Estado de São Paulo (FAPESP, Brazil; Fundação para a Ciência e a Tecnologia (FCT, Portugal)

In many male vertebrates, the secretion of reproductive (gonadal androgens) and adrenocortical (glucocorticoids) hormones varies seasonally and in response to environmental stimuli, and these hormones exert numerous behavioral and metabolic effects. We performed two field studies on adult male Rufous-winged Sparrows, Peucaea carpalis, a Sonoran Desert rain-dependent sedentary species, to (a) determine seasonal changes in initial (baseline) and acute stress-induced plasma testosterone (T), corticosterone (CORT), and two metabolites (uric acid and glucose) and (b) compare the effects of two types of social challenge (song playback or simulated territorial intrusion consisting of song playback plus exposure to a live decoy bird) on plasma T, CORT, these metabolites, and territorial behavior. Initial plasma T was higher during the summer breeding period than during post-breeding molt. Acute stress resulting from capture and restraint for 30 min decreased plasma T in breeding condition birds but not in the fall, revealing that this decrease is seasonally regulated. Initial plasma CORT did not change seasonally, but plasma CORT increased in response to acute stress. This increase was likewise seasonally regulated, being relatively smaller during autumnal molt than in the summer. We found no evidence that acute stress levels of CORT are functionally related to stress-depressed plasma T and, therefore, that plasma T decreases during stress as a result of elevated plasma CORT. Thirty minutes of exposure to simulated territorial intrusion resulted in different behavior than 30 min of exposure to song playback, with increased time spent near the decoy and decreased number of overhead flights. Neither type of social challenge influenced plasma T, thus offering no support for the hypothesis that plasma T either responds to or mediates the behavioral effects of social challenge. Exposure to both social challenges elevated plasma CORT, but simulated territorial intrusion was more effective in this respect than song playback. Plasma uric acid and glucose decreased during acute stress, but only plasma uric acid decreased during social challenge. Thus, an elevation in plasma CORT was consistently associated with a decrease in plasma uric acid, but not with a change in glycemia. These results enhance our understanding of the short-term relationships between T, CORT, and avian territorial behavior. They provide novel information on the endocrine effects of acute stress, in particular on plasma T, in free-ranging birds, and are among the first in these birds to link these effects to metabolic changes.

Many animals adapt to rapidly changing social environments by using social information to modulate their hormone titres. Modulation of hormone titres, as proposed by the challenge hypothesis, provides a mechanism by which individuals can match their behaviour to their current social environment and thereby avoid costs associated with prolonged high hormone titres. Thus far, most work on social responsiveness of hormone titres has focused on androgens in vertebrates. However, there is mounting evidence that insect hormones, especially juvenile hormone, may respond to social stimuli in ways that parallel androgens in vertebrates. This review will integrate work on social modulation of hormone titres in vertebrates and insects. First we review how the hormone-mediated trade-off between fecundity and life span may be a key selective force favouring socially responsive hormone titres in both systems. Then we review theoretical and empirical work in vertebrates and insects that address how factors such as social instability, dominance rank and mating system influence hormone titre responsiveness. These studies illustrate that (1) juvenile hormone (JH) is responsive to social stimuli in a range of insect taxa and (2) JH responses match key predictions of the challenge hypothesis. We conclude that there are strong similarities in endocrine responsiveness across vertebrate and insect taxa. The challenge hypothesis provides a useful conceptual framework for hypothesis-driven research in insect endocrinology. In addition, exploring areas of convergence and divergence across vertebrates and insects may help clarify how selection has shaped patterns of endocrine responsiveness.

The challenge hypothesis posits that male testosterone levels increase in the presence of fertile females to facilitate mating and increase further in the presence of male rivals to facilitate male–male competition. This hypothesis has been supported in a number of nonhuman animal species. We conducted an experiment to test the challenge hypothesis in men. Thirty-four men were randomly assigned to view high-competitive or low-competitive male rivals at high and low fertility within their partner's ovulatory cycle (confirmed by luteinizing hormone tests). Testosterone was measured upon arrival to the lab and before and after the manipulation. Based on the challenge hypothesis, we predicted that a) men's baseline testosterone would be higher at high relative to low fertility within their partner's cycle, and b) men's testosterone would be higher in response to high-competitive rivals, but not in response to low-competitive rivals, at high relative to low fertility within their partner's cycle. Contrary to the first prediction, men's baseline testosterone levels did not differ across high and low fertility. However, consistent with the second prediction, men exposed to high-competitive rivals showed significantly higher post-test testosterone levels at high relative to low fertility, controlling for pre-test testosterone levels. Men exposed to low-competitive rivals showed no such pattern (though the fertility by competition condition interaction fell short of statistical significance). This preliminary support for the challenge hypothesis in men builds on a growing empirical literature suggesting that men possess mating adaptations sensitive to fertility cues emitted by their female partners.

The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The hypothesis has been tested many times over the past 30years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.

Few studies have investigated the influence of changes in testosterone on subsequent competitive, antagonistic behavior in humans. Further, little is known about the extent to which such effects are moderated by personality traits. Here, we collected salivary measures of testosterone before and after a rigged competition. After the competition, participants were given the opportunity to act antagonistically against the competitor (allocate a low honorarium). We hypothesized that changes in testosterone throughout the competition would predict antagonistic behavior such that greater increases would be associated with the allocation of lower honorariums. Further, we investigated the extent to which personality traits related to psychopathy (fearless dominance, FD; self-centered impulsivity, SCI; and coldheartedness) moderated this relationship. In men (n=104), greater increases in testosterone and greater FD were associated with more antagonistic behavior, but testosterone concentrations did not interact with personality measures. In women (n=97), greater FD and SCI predicted greater antagonistic behavior, but there were no significant endocrine predictors or interactions with personality measures. In a secondary set of analyses, we found no support for the dual-hormone hypothesis that the relationship between baseline testosterone concentrations and behavior is moderated by cortisol concentrations. Thus, results are consistent with previous findings that in men, situation-specific testosterone reactivity rather than baseline endocrine function is a better predictor of future antagonistic behavior. The results are discussed with respect to the Challenge Hypothesis and the Biosocial Model of Status, and the possible mechanisms underlying the independent relations of testosterone and personality factors with antagonistic behavior.

To compete for parental food deliveries nestling birds have evolved diverse behaviors such as begging displays and sibling aggression. Testosterone has been suggested to be an important mechanism orchestrating such competitive behaviors, but evidence is scarce and often indirect. Siblicidal species provide an interesting case in which a clear dominance hierarchy is established and the dominant chicks lethally attack siblings. We experimentally elevated testosterone in chicks of a facultatively siblicidal species, the black-legged kittiwake, Rissa tridactyla, and showed that testosterone-treated chicks were more aggressive toward their sibling than were control chicks. In such facultatively siblicidal species, chicks normally exhibit intense aggression only when threatened by starvation. Indeed, we found that chicks in relatively poorer condition were more aggressive than were chicks in better condition, even among testosterone-treated chicks, suggesting the action of an additional signal modulating aggression. Relatively larger siblings were also more aggressive than were relatively smaller siblings, confirming the importance of size advantage in determining dominance hierarchies within the brood. In addition, testosterone increased aggression toward a simulated predator, indicating that in kittiwakes testosterone can increase aggression in contexts other than siblicide. Testosterone promoted aggression-mediated dominance, which increased begging although testosterone treatment did not have a significant separate effect on begging. Therefore, testosterone production in the kittiwake and most likely other siblicidal species seems an important fitness mediator already early in life, outside the sexual context and not only manifesting itself in aggressive behavior but also in dominance-mediated effects on food solicitation displays toward parents.

article i nfo Article history: Initial receipt 5 March 2013 Final revision received 19 June 2013 Testosterone plays an important role in mediating male reproductive trade-offs in many vertebrate species, augmenting muscle and influencing behavior necessary for male-male competition and mating-effort. Among humans, testosterone may also play a key role in facilitating male provisioning of offspring as muscular and neuromuscular performance is deeply influenced by acute changes in testosterone. This study examines acute changes in salivary testosterone among 63 Tsimane men ranging in age from 16 to 80 (mean 38.2) years during one-hour bouts of tree-chopping while clearing horticultural plots. The Tsimane forager- horticulturalists living in the Bolivian Amazon experience high energy expenditure associated with food production, have high levels of parasites and pathogens, and display significantly lower baseline salivary testosterone than age-matched US males. Mixed-effects models controlling for BMI and time of specimen collection reveal increased salivary testosterone (p b 0.001) equivalent to a 48.6% rise, after one hour of tree chopping. Age had no effect on baseline (p = 0.656) or change in testosterone (p = 0.530); self-reported illness did not modify testosterone change (p = 0.488). A comparison of these results to the relative change in testosterone during a competitive soccer tournament in the same population reveals larger relative changes in testosterone following resource production (tree chopping), compared to competition (soccer). These findings highlight the importance of moving beyond a unidimensional focus on changes in testosterone and male-male aggression to investigate the importance of testosterone-behavior interactions across additional male fitness-related activities. Acutely increased testosterone during muscularly intensive horticultural food production may facilitate male productivity and provisioning.

An accumulation of evidence suggests that increased exposure to androgens is associated with prostate cancer risk. The unrestricted energy budget that is typical of Western diets represents a novel departure from the conditions in which men's steroid physiology evolved and is capable of supporting distinctly elevated testosterone levels. Although nutritional constraints likely underlie divergent patterns of testosterone secretion between Westernized and non-Western men, considerable variability exists in men's testosterone levels and prostate cancer rates within Westernized populations. Here, I use evolutionary life history theory as a framework to examine prostate cancer risk. Life history theory posits trade-offs between investment in early reproduction and long-term survival. One corollary of life history theory is the 'challenge hypothesis', which predicts that males augment testosterone levels in response to intrasexual competition occurring within reproductive contexts. Understanding men's evolved steroid physiology may contribute toward understanding susceptibility to prostate cancer. Among well-nourished populations of Westerners, men's testosterone levels already represent an outlier of cross-cultural variation. I hypothesize that Westernized men in aggressive social environments, characterized by intense male-male competition, will further augment testosterone production aggravating prostate cancer risk.

Although testosterone (T) has well known organizational and activational effects on aggression, the relationship between the two is not always clear. The challenge hypothesis addresses this problem by proposing that T will affect aggression only in fitness-enhancing situations. One way to test the challenge hypothesis is to examine the relationship between T and different types of aggression. Chimpanzees, Pan troglodytes, show aggressive behaviours in several contexts and provide an opportunity for such a test. Here we show that urinary T influences a form of male chimpanzee reproductive aggression, territorial boundary patrols. In contrast, T does not affect predatory behaviour, a form of aggression that has no immediate link to male reproduction. While these results are consistent with the challenge hypothesis, our results indicate that male chimpanzees experience a significant drop in urinary T during hunts. Additional analyses reveal that males who share meat with others display this decrease. The reason for this decrement is unclear, but we hypothesize that the relative lack of aggression that results from voluntary sharing episodes and the tolerance engendered by such acts may be contributory factors.

Social challenges from rival conspecifics are common in the lives of animals, and changes in an animal’s social environment can influence physiology and behavior in ways that appear to be adaptive in the face of continued social instability (i.e. social priming). Recently, it has become clear that testosterone, long thought to be the primary mediator of these effects, may not always change in response to social challenges, an observation that highlights gaps in our understanding of the proximate mechanisms by which animals respond to their social environment. Here, our goal is to address the degree to which testosterone mediates organismal responses to social cues. To this end, we review the behavioral and physiological consequences of social challenges, as well as their underlying hormonal and gene regulatory mechanisms. We also present a new case study from a wild songbird, the dark-eyed junco Junco hyemalis, in which we find largely divergent genome-wide transcriptional changes induced by social challenges and testosterone, respectively, in muscle and liver tissue. Our review underscores the diversity of mechanisms that link the dynamic social environment with an organisms’ genomic, hormonal, and behavioral state. This diversity among species, and even among tissues within an organism, reveals new insights into the pattern and process by which evolution may alter proximate mechanisms of social priming.

Decades of behavioral endocrinology research have shown that hormones and behavior have a bidirectional relationship; hormones both influence and respond to social behavior. In contrast, hormones are often thought to have a unidirectional relationship with ornaments. Hormones influence ornament development, but little empirical work has tested how ornaments influence hormones throughout life. Here, we experimentally alter a visual signal of fighting ability in Polistes dominulus paper wasps and measure the behavioral and hormonal consequences of signal alteration in signalers and receivers. We find wasps that signal inaccurately high fighting ability receive more aggression than controls and receiving aggression reduces juvenile hormone (JH) titers. As a result, immediately after contests, inaccurate signalers have lower JH titers than controls. Ornaments also directly influence rival JH titers. Three hours after contests, wasps who interacted with rivals signaling high fighting ability have higher JH titers than wasps who interacted with rivals signaling low fighting ability. Therefore, ornaments influence hormone titers of both signalers and receivers. We demonstrate that relationships between hormones and ornaments are flexible and bidirectional rather than static and unidirectional. Dynamic relationships among ornaments, behavior, and physiology may be an important, but overlooked factor in the evolution of honest communication.

Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high-ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10-month period in relation to rank, age, natal status, and group tenure length, including during a socially unstable period in which coalitions of lower ranked males attacked higher ranked males. Androgen, but not GC, levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High-ranking male targets had the highest GC levels of all males when targeted and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.

Recent research points to decreasing testosterone (T) levels as well as decreasing relationship quality during the transition to fatherhood, and it has been suggested that T reflects and affects motivation and behavior with respect to mating or paternal effort. Accordingly, we hypothesized that decreases in T are associated with decreasing relationship quality in new fathers. Thirty-seven fathers and 38 men in committed romantic relationships without children (controls) were recruited. All subjects participated actively by collecting saliva samples for T assessment three times a day on two assessment days, four weeks prior to birth (day 1) and eight weeks after birth (day 2) for fathers, and three months after the first assessment for controls and by filling out questionnaires on relationship quality. Results revealed significantly lower T levels (AUCg-T) in fathers than in controls at day 2 and significant decreases in relationship quality from day 1 to day 2 in fathers, but not in controls. In particular, the new fathers reported tenderness in their relationship to have significantly decreased from pre to post birth in comparison to the controls. These results were partially moderated by T levels at day 1. We interpret our results as being in line with the "challenge hypothesis" in humans, according to which T levels are positively associated with mating effort and negatively related to paternal activities.

Male song sparrows (Melospiza melodia) are territorial year-round. However, neuroendocrine responses to simulated territorial intrusions (STI) differ between breeding (spring) and non-breeding seasons (autumn). In spring, exposure to STI leads to increases in plasma levels of luteinizing hormone and testosterone (consistent with the challenge hypothesis), but not in autumn. This suggests that there are fundamental differences in the mechanisms driving neuroendocrine responses to STI between seasons despite apparently identical behavioral responses. Recent studies have also shown that areas of the telencephalon and diencephalon involved with singing behavior and aggression express the enzymes necessary to synthesize sex steroids de novo from cholesterol. Of these, aromatase (that regulates the conversion of testosterone to estradiol) and 3β-hydroxysteroid dehydrogenase (that regulates the synthesis of biologically active steroids) are regulated seasonally, whereas receptors for sex steroids such as androgen receptor and estrogen receptor alpha and beta are not. Functional analyses indicate specific genes that may be involved in the mechanisms of differential neuroendocrine responses to aggressive interactions in different life-history stages. Microarrays were used to test the hypothesis that gene expression profiles in the hypothalamus after territorial aggression differ between the seasons. Over 150 genes were differentially expressed between spring and autumn in the control birds and 59 genes were significantly affected by STI in autumn, but only 14 genes in spring. Real-time PCR was performed for validation, and it indicated that STI drives differential genomic responses in the hypothalamus in the breeding versus non-breeding seasons. The results suggest major underlying seasonal effects in the hypothalamus that determine the differential response upon social interaction.