Opinion TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 Social dominance and stress hormones Scott Creel In most cooperatively breeding birds and mammals, reproductive rates are lower for social subordinates than for dominants, and it is common for reproduction in subordinates to be completely suppressed. Early research conducted in captivity showed that losing fights can increase glucocorticoid (GC) secretion, a general response to stress. Because GCs can suppress reproduction, it has been widely argued that chronic stress might underlie reproductive suppression of social subordinates in cooperative breeders. Contradicting this hypothesis, recent studies of cooperative breeders in the wild show that dominant individuals have elevated GCs more often than do subordinates. The findings that elevated GCs can be a consequence of subordination or a cost of dominance complicate the conventional view of social stress, with broad ramifications for the evolution of dominance and reproductive suppression. Animals respond to a stressor with a series of endocrine responses that increases the immediate availability of energy, in part by inhibiting physiological processes that are not required for immediate survival1–3. One of the primary responses to stress is an increase in the activity of the hypothalamic–pituitary–adrenocortical axis, causing an increase in the concentration of circulating adrenal glucocorticoids (GC). In the short term (hours to days), GC elevations redirect resources to mobilize energy that can be used to resolve the stressful situation2. If the stressor is not eliminated, and GC levels remain high for more than a few days, a broad range of harmful consequences ensue, including immune suppression, loss of muscle mass and reproductive suppression2,4,5. 491 There is a tendency to consider any difficult or energetically demanding situation a stressor. As Wingfield and Ramenofsky6 point out: ‘phrases such as “the stress of reproduction’’ or “the stress of migration”… are inaccurate, because these processes occur on predictable schedules and an individual can make necessary preparations’. In a broad sense, one might consider reproduction as a stressor, because reproducing entails activities and costs that make it more difficult than not reproducing. Under the narrower definition given above, reproduction or migration should not automatically be considered stressful simply because they are difficult. Difficult conditions, whether they are physical or psychological, often do not provoke a physiological stress response unless they are unpredictable or uncontrollable. The importance of predictability and control has been shown very neatly in experiments with rats Rattus norvegicus9. For example, two rats can be put in a divided cage with a shock grid on the floor, so that both are subject to the same series of electric shocks. If one rat can decrease the rate of shocks by pressing a lever, the rat without the lever (without control) typically has a larger GC response, in spite of facing an identical physical challenge. Defining stress Scott Creel Dept of Ecology, Montana State University, Bozeman, M 59717, USA. e-mail: [email protected] Even among biologists, the word ‘stress’ has many meanings6. It can be used to refer to the condition provoking a response (a stressor), and to refer to changes in internal state induced by the external condition (a stress response). It is generally clearer to avoid the word stress, and refer explicitly to stressors and stress responses. For the purposes of this review, a stressor is any stimulus (behavioral, environmental, or demographic) that provokes a physiological stress response, as measured by an increase in GC secretion. Although other physiological systems also respond directly to stressors, GC responses have been studied in a broad range of species, including some in the wild. In addition, the physiological and behavioral effects of GCs are relatively well characterized2,4 relative to other stress responses, for example, the production of heat shock proteins7. Even for GCs, there is considerable debate about the physiological and behavioral consequences of increased secretion3, and responses to GC elevation vary among individuals and species8. http://tree.trends.com Fig. 1. Examples of agnostic interaction. Agonistic and aggressive behaviors are similar in most social carnivores, even those that are distantly related. A winner and loser can be assigned, and used to estimate social status. (a) African wild dog Lycaon pictus greeting by two subordinates as a dominant individual approaches. The dog in the foreground is sending mixed signals of dominance (tail up and fanned) and subordination (play bow). (b) A dominant dwarf mongoose Helogale parvula pins a subordinate to the ground as it rolls onto its back in submission. 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02227-3 492 Opinion TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 Table 1. Relationships between basal glucocorticoid levels and social status within cooperatively breeding groupsa,b Species Sex Rodents Naked mole-rat Heterocephalus glabe Social system Reproductive suppression of subordinatesc Captive or wild study Method of sampling GCs Notes Refs F and M Sub > Dom Social and cooperative High skew Captive Urine Long-term studies 30 M Dom > 3 types, of sub Dom < 1 type of sub Social and cooperative Low skew Wild Blood: long and variable lag from trapping to sample Categorized subs by yearling–adult and son–nonson 24 F Dom > Sub Social and cooperative High skew Captive Blood 28 Black tufted-ear marmoset Callithrix kuhli F Dom = Sub High skew Captive Urine 33 M Dom > Sub Social and cooperative Social and cooperative High skew Captive Urine Ring-tailed lemur Lemur catta F Dom > Sub Social and cooperative Low skew Wild Feces 25 Cotton-top tamarin Saguinus oedipus F Paired > Sub with M Social and cooperative High skew Captive Urine 34 F and M Dom = Sub Social and cooperative Low skew Wild Blood Very low GC levels for all ranks 21 Social and cooperative Social and cooperative Low skew Wild Blood During all nest stages 22 Low skew Wild Blood Dom > Sub at mating stage 35 Alpine marmot Marmota marmota Primates Common marmoset Callithrix jacchus Birds White-browed sparrow weaver Plocepasser mahali Basal GC pattern Additional data from J. French Florida scrub jay Aphelocoma coerulescens F Dom > Sub M Dom = Sub Harris' hawk Parabuteo unicinctus F and M Dom = Sub (see notes) Social and cooperative High skew Wild Blood NS ANOVA for GC in breeders, auxiliaries and juveniles 35 Carnivores Wolf Canis lupus F and M Dom = Sub Social and cooperative High skew Captive Blood In wild packs, Dom > Sub 36 F Dom > Sub Social and cooperative High skew Wild Urine Acute GC: Dom > Sub 14,26 M Dom = Sub Social and cooperative High skew Wild Urine Acute GC: Dom < Sub F and M Dom > Sub Social and cooperative High skew Dwarf mongoose Helogale parvula African wild dog Lycaon pictus Wild Feces 15,26 aThis excludes studies in which individuals in different groups or on different territories are compared, for example comparisons of unmated, monogamously mated and polygynously mated male birds on neighboring breeding territories. bAbbreviations GC, glucocorticoid; NS, not significant at P = 0.05. cHigh skew refers to species in which reproductive success is highly skewed within groups (subordinates rarely breed); Low skew, species in which subordinates often breed. Similarly, two rats can be subjected to an identical series of shocks, but one is given a warning sound before the shocks so that they are predictable, which significantly reduces its GC response9. Because of the impact of predictability and control on GC responses, behavioral interactions can be potent stressors (Fig. 1). For over 30 years, it has been known that aggressive or agonistic interactions can provoke large and persistent increases in GC secretion. Influential early work on this issue was conducted with captive rodents and primates, often by grouping unfamiliar individuals, observing the fights that ensued and comparing the GC levels of winners and losers10–12. In this situation, both winners and losers showed a strong stress response, but the response was larger among losers. In these http://tree.trends.com early studies, losers were generally called ‘subordinates’, and winners were called ‘dominants’. These studies are the origin of the conventional view that social subordination is stressful. Winner–loser contests and naturally formed hierarchies These were ground-breaking studies that revealed much about the associations between aggressive behavior and stress responses. However, such studies do not necessarily reveal the consequences of living as a subordinate in a social group that has a settled dominance hierarchy. The rate and severity of fighting are high immediately after strangers are grouped, particularly among males, which were the focus of most of the winner–loser studies. Opinion TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 493 Table 2. Relationships between basal glucocorticoid levels and social status within groups that do not breed cooperatively, and in winner–loser studiesa,b Species Sex Basal GC pattern Social system Reproductive suppression of subordinatesc Captive or wild study Method of sampling GCs Notes Refs Rodents Mouse Mus musculus M Sub > Dom Solitary ancestral No Captive Blood Winner–loser studies 10,11 Rat Rattus norvegicus M Sub > Dom Solitary ancestral No Captive Blood Short- and long-term studies 37 Primates Squirrel monkey Saimiri sciureus M M Sub > Dom Dom > Sub Social Social No No Captive Captive Blood Blood See next study See previous study 12,38 Rhesus macaque Macaca mulatta M Dom = Sub Social No or low skew Captive (enclosure) Blood 0.3 Ha enclosure 39 Lesser mouse lemur Microcebus murinus M Dom = Sub Solitary Low skew Captive Blood Olive baboon Papio anubis M Sub > Dom Social Low skew Wild Blood F and M Sub > Dom Summer pairs, winter flocks No Wild Blood 41 F and M Sub > Dom Summer pairs, winter flocks No Wild Blood 42 F Solitary, ancestral No or low skew Captive Saliva Birds Harris’ sparrow Zonotrichia querula White-throated sparrow Zonotrichia albicollis Suids Domestic pig Sus scrofa Sub > Dom 40 Only with stable hierarchy Dom/Sub = ‘high–low success’ 2,32 43 aThis excludes studies in which individuals in different groups or on different territories are compared, for example comparisons of unmated, monogamously mated and polygynously mated male birds on neighboring breeding territories. bAbbreviations GC, glucocorticoid; NS, not significant at P = 0.05. cHigh skew refers to species in which reproductive success is highly skewed within groups (subordinates rarely breed); Low skew, species in which subordinates often breed. Number of cases For example, Blanchard et al.13 put 100 male rats in a system of clear tunnels and recorded their behavior, along with changes in body mass and plasma GC levels. Initially, rates of fighting exceeded 40 fights per hour, for both dominants and subordinates. After 13 days, subordinates had an average of 17 body wounds, and had lost more than 20% of their initial body mass, in spite of being removed from the colony on four days to feed for eight hours. Aggression this severe would be unusual for a social species in the wild, where agonistic encounters rarely escalate to the point of wounding and rates of aggression are lower14,15. Indeed, it is 9 8 7 6 5 4 3 2 1 0 D>S D=S S>D D>S D=S S>D Relationship between rank and GCs TRENDS in Ecology & Evolution Fig. 2. The relationship between basal glucocorticoid (GC) levels and social status in species with cooperative breeding (purple bars) and in other social systems (yellow bars). D and S represent dominant and subordinate: D > S means that GC levels were significanty higher in dominant individuals, D = S means that GC levels are not detectably affected by rank, and S > D means that GC levels were significantly higher in subordinates. http://tree.trends.com generally thought that social dominance evolves to avoid the costs and risks of escalated fights, when the outcome can be reliably predicted16. Perhaps work on GC responses of winners and losers could be related to the social events that follow immigration or group formation in the wild, when social relationships are often established through fighting17–19. Captive winner–loser studies do not necessarily predict relationships between social status and basal stress hormone levels for stable social groups in the wild, because of substantial differences in social context. A set of recently paired males in a small enclosure differs in many ways from a wild group (often formed of relatives) that has formed by recruitment of offspring over many years, with individuals free to disperse if they choose. Captive subordinates cannot avoid dominant individuals as effectively as they would be able to in the wild. In the wild, moving away is a common means of terminating an attack if behavioral appeasement does not work. Of course, the ultimate form of moving away from dominant individuals is dispersal, an option not open to captive animals. In spite of these complexities, captive winner–loser studies are the original basis of the common argument that the ‘stress of subordination’ or ‘psychological castration’ might underlie reproductive suppression among subordinates in cooperatively breeding species20–22. Given this, it is interesting to ask what recent studies reveal about the endocrine consequences of rank in social species, particularly in cooperative breeders. Opinion 494 TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 Box 1. Types of dominants and subordinates Glucocorticoid concentration (ng g–1 dry feces) I (a) 6.5 5.5 4.5 3.5 2.5 1.5 Nonresponder Responder Post-hoc classification 24 Number of observations (b) 20 16 12 8 4 0 –1 0 1 2 3 4 5 6 7 8 9 Glucocorticoid concentration (ng g–1 dry feces) TRENDS in Ecology & Evolution When a difference exists between dominants and subordinates in circulating glucocorticoid (GC) concentrations, it is possible that the difference is not a result of social status itself, but of some other trait that varies among individuals of different ranks. Such traits might also vary among individuals of similar rank, and several studies have noted that dominants or subordinates of different behavioral types differ in their basal GC levelsa–c. For example, Blanchard et al.d found that, in comparison to dominant rats, subordinates had higher basal GC concentrations and lower acute GC levels in response to the stress of restraint. They then ranked subordinates by the strength of their acute GC response, classifying subordinates as ‘responders’ or ‘nonresponders’, and showed that there was a pronounced difference between the two groups in acute GC response, as shown for simulated data in Fig. Ia. They then demonstrated that responders and nonresponders differed significantly in some aspects of behavior. From Fig. Ia, it appears obvious that there are fundamental differences between nonresponders and responders: they are two distinct types, and the underlying frequency distribution of acute GC concentrations is bimodal. This is not a safe conclusion. For these data, the apparent existence of two types of subordinates is entirely a result of the process of post-hoc classification. The underlying frequency distribution is a Gaussian distribution with µ = 4 and σ = 2, from which 100 random values were drawn (Fig. Ib) to create the data for Fig. Ia. Through post hoc separation of the left and right halves of the distribution, it appears that two classes of subordinates exist (Fig. Ia), when the distribution of GC responses is actually unimodal. This example shows that the conclusion that several types or ‘styles’ of dominant or subordinate exist is sometimes not well supported by data. Of course, this does not mean that multiple types do not exist. For example, Virgin and Sapolskyb classified subordinate baboons on the basis of behavioral traits, rather than making a post hoc classification on the basis of GC levels, and found that some traits were good predictors of acute GC responses (but were not good predictors of basal GC levels). References a Kotrschal, K. et al. (1998) The relationship between social stress and dominance is seasonal in greylag geese. Anim. Behav. 55, 171–176 b Virgin, C.E. and Sapolsky, R.M. (1997) Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am. J. Primatol. 42, 25–39 c Mendl, M. et al. (1992) Phsyiological and reproductive correlates of behavioural strategies in female domestic pigs. Anim. Behav. 44, 1107–1121 d Blanchard, D.C. et al. (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20, 117–134 Endocrine correlates of rank in social species Tables 1 and 2 summarize 25 studies that relate basal GC concentrations to rank. These studies used variable methods, which probably affected their results to some (unknown) degree. For cooperative breeders, the list is complete. Of the 25 studies, eight found that basal GC levels were significantly higher among subordinates, eight found that GC levels were significantly higher among dominants, and eight failed to detect an effect of social status. Based simply on the number of studies that have found each broad pattern, there is often an association between basal GCs and rank (64% of the studies), but it was equally common for dominants and subordinates to be the class in which basal GC levels are elevated. The eight cases in which dominants had the higher basal GCs share one obvious similarity: all were cooperative breeders (Fig. 2). Five of these studies were conducted with naturally assembled groups in http://tree.trends.com the wild. By contrast, only one of the eight cases in which subordinates had higher GC levels came from a cooperative breeder, and five of these studies were conducted in captivity. Considering cooperative breeders only, GCs were higher in dominants in eight cases (nine if the cotton-top tamarin Saguinus oedipus is included, where subordinates were compared to monogamously mated females), equal in six cases, and higher in subordinates in two cases. (This includes olive baboons Papio anubis; if one classifies baboons as social but not cooperative, then GCs were higher insubordinates only for captive naked mole rats Heterocephalus glaber among the cooperative breeders.) Narrowing further still to studies of cooperative breeders in the wild, five cases support the hypothesis that it is stressful to be dominant, whereas one supports the hypothesis that it is stressful to be subordinate. Opinion TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 495 Box 2. Chronic and acute stress Although the terminology is cumbersome, there is an important distinction between short-term (‘acute’) and long-term (‘chronic’) stress responses. When exposed to a stressor, a typical individual will mount a pronounced glucocorticoid (GC) response within two to ten minutes. During this acute response, circulating GC levels typically rise several fold, but drop back to basal levels minutes (or perhaps a few hours) after the stressor is removed. This short-term response is generally considered adaptive, because it shifts energy and resources away from physiological processes that can be curtailed briefly without harm, putting these resources instead toward resolving the stressful condition. By contrast, if an elevation of GCs persists for days or weeks, then many of the short-term benefits become long-term pathologies, including immune suppression, reproductive suppression, gastric ulcers and muscle wasting. Sapolskya provides an excellent review of the short-term benefits and long-term harms that elevations of GCs usually provoke, and their mechanisms. Because of the dichotomy in the effects of acute and chronic GC responses, studies of social stress generally focus on chronic elevations of GCs (elevated basal values). Some studies go further by also testing for effects of social status on acute GC responsesb–d. When basal GC concentrations are elevated, a common consequence is a weakening of the acute GC responsed, probably through changes in negative feedback mechanisms in the hypothalamic–adrenal– pituitary axis. This is an endocrine vicious circle: a chronically high baseline can provoke pathologies, and a weak acute response is ineffective at handling short-term stressorse. References a Sapolsky, R.M. (1992) Neuroendocrinology of the stress response. In Behavioral Endocrinology (Becker, J.B. et al., eds), pp. 287–324, Massachusetts Institute of Technology Press b Schoech, S. et al. (1991) Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida scrub jays (Aphelocoma c. coerulescens). Condor 93, 354–364 c Creel, S. et al. (1996) Social stress and dominance. Nature 379, 212 d McEwen, B.S. and Schmenk, H.M. (1994) The Hostage Brain, Rockefeller University Press e Virgin, C.E. and Sapolsky, R.M. (1997) Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am. J. Primatol. 42, 25–39 From Tables 1 and 2, (two) general conclusions can be drawn. First, the relationship between basal GCs and rank is highly variable. Variables that might affect the strength and direction of this relationship include the social system, domestication, phylogeny, the behavioral traits that are associated with high and low rank, and whether the study was conducted in the wild or in captivity (Box 1). Second, although the data are still sparse for the purposes of comparative analysis, it is uncommon for subordinates of species that live in permanent groups to experience chronically elevated GCs (Fig. 1). Only one study of a social species in the wild has found elevated basal GCs in subordinates23, whereas five field studies have found higher levels in dominants. These five cases are phylogenetically well distributed, including a bird (Florida scrub jay Aphelocoma coerulescens)22, a rodent (alpine marmot Marmota marmota)24, a primate (ring tailed lemur Lemur catta)25 and two carnivores (dwarf mongoose Helogale parvula and African wild dog Lycaon pictus)15,26. The interpretation of differences among ranks in GC levels is not entirely clear-cut. A priori, the class of individuals with higher basal GCs would generally be considered more socially stressed. However, data from captive common marmosets27,28 show that GC levels do not increase upon attaining dominance: rather, GC levels decrease among subordinates, in parallel with estrogen levels. Field studies have not generally tested whether the differences between ranks arise through increased GC secretion in one class or reduced secretion in the other class, although limited data from African wild dogs and dwarf mongooses show that GC levels increase upon attaining dominance. Considering the impact of GCs on fitness, the difference in mechanisms might be moot, if the social class with higher basal GC levels is exposed to more of their harmful effects. http://tree.trends.com Implications and future research If dominant animals do generally have elevated GC levels among cooperative breeders, this would represent a major shift in our view of social stress. We must consider the stress of domination, as well as the stress of subordination, and how these stressors might affect social evolution. There are several interesting questions to address. First, what behavioral differences among species (Box 2) predict whether stress will fall more heavily on dominants or on subordinates (or perhaps on midranking animals, in some cases)? This is already an active field of study25,29, and two possibilities are that dominants have elevated GCs when a hierarchy is unstable2 or in species in which dominants fight more often than do subordinates26. Second, what are the nonGC-mediated mechanisms by which rank affects sexual behavior and sex steroid levels? It is already clear that reproductive suppression is not mediated by chronic GC elevation for most of the cooperative breeders that have been studied (Table 1, species listed as ‘high skew’). However, many aspects of reproductive behavior and sex-steroid secretion are depressed in subordinates of these species14,15,22,30. Considering the broad range of pathologies that chronic GC elevations can cause2,4, it is perhaps not surprising that reproductive suppression is rarely GC mediated in species for which reproductive suppression is a normal feature of social organization. With such a social system, stress-mediated mechanisms of suppression would be evolutionarily invasible by a direct mechanism of suppression that did not involve GC elevation, and thus avoided the costs of immune suppression and other pathologies. If this line of reasoning is correct, stress-mediated 496 Opinion TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 Box 3. Field studies and noninvasive sampling: strengths and weaknesses When research examines interactions between the social environment and endocrine function, there are obvious benefits to conducting studies in the wild. By gathering data from naturally assembled groups in their normal context, one can eliminate concerns about the effects of crowding, constant interaction, imposed group compositions and limited dispersal options. With these benefits come some problems. Notably, experimental control of variables other than the social environment becomes difficult, so one must rely on statistical controls. Some of the strength of field endocrinology can be lost by invasive sampling. In traditional lab studies, blood samples are taken to measure circulating glucocorticoid (GC) levels. To collect blood in the field, capture is required for all species and anesthesia is required for large or dangerous species. Capture creates two potential problems for a study of stress physiology. First, circulating GC levels will increase within minutes of darting or capture, and this interferes with the measurement of a true, accurate baseline unless there is a short and consistent interval from first disturbance to blood sampling. Second, even if animals can be captured and sampled quickly, the procedure constitutes a stress. If repeated often, the stress of capture could affect the processes under study. To reduce or eliminate capture stress, some studies rely on noninvasive measurement of GC levels in urine and feces. When compared with traditional measurements from serum or plasma, urinary or fecal measurements have several weaknesses, but also some strengths. Steroid hormones exert their effects by binding to receptors, and circulating levels are a closer indication of receptor binding than are excreted levels. Even circulating steroid measurements are complicated by variation in the amount of steroid-binding globulin and by variation in receptor densities. Urinary or fecal measurements can be complicated by individual variation in the diet, or in clearance of hormones by the kidney or liver. Methods to lessen these problems include controlling for variation in the concentration of urine by measuring creatinine concentrationa, and controlling for the water content and amount of indigestible material in fecesb,c. Nonetheless, hormone profiles based on urinary and especially fecal measurements are typically noisier than are profiles from serum or plasma. Consequently, noninvasive studies might require larger sample sizes to detect how reproductive suppression might only be expected in primitively social species, or in species where suppression is a reaction to unusually high population density. Finally, the observation that dominants experience chronic elevations of GCs in many cooperative breeders has implications for the evolution of dominance itself. If social stress falls most heavily on dominants, and if high basal GC levels carry a fitness cost through effects on energy metabolism and immune function2, then being dominant is not as beneficial as it might at first appear. Hidden physiological costs might accompany the access to mates and resources that dominant individuals enjoy. If so, this would help to explain why subordinates accept their status with perplexing readiness. For example, age is a common covariate of social rank31. It is easy to understand that the body mass and experience gained with age would be of benefit for young adults, but it is harder to understand why age remains a good predictor of rank among old animals. In dwarf mongooses Helogale parvula, an alpha female that was physically feeble at http://tree.trends.com social or demographic conditions affect GC levels. However, steroid hormone levels fluctuate on short time scales, and measurements from blood are essentially instantaneous samples from a constantly shifting baseline. For example, normal diurnal fluctuations in GC concentrations can be as high as sevenfoldd. A study of the effect of social status on basal GC levels would ideally take a moving average of short-term fluctuations in GCs. Urinary and fecal samples have this pooling effect, by integrating changes in hormone secretion for the period over which a given defecation or urination was pooled. References a Erb, R.E. et al. (1970) Urinary creatinine as an index compound for estimating rate of excretion of steroids in the domestic sow. J. Anim. Sci. 30, 79–85 b Wasser, S.K. et al. (1993) Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J. Reprod. Fert. 97, 569–574 c Monfort, S.L. (1997) Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus). Zoo Biol. 16, 533–548 d Saito, M. and Kato, H. (1985) Circadian anticipatory response to food intake in behavioral and endocrine functions. In Circadian Clocks and Zeitgebers (Hioshige, T. and Houma, K., eds), pp. 146–156, Hokkaido University Press 13 years of age remained clearly dominant to seven other adult females ranging in age from 2 to 11 years (S. Creel, pers. observ.). Although this is just one case, it exemplifies the general pattern that age explains much of the variance in rank for dwarf mongooses14 and many other cooperative breeders31. Adults well beyond the age of maturity accept subordination simply on the basis of age, even though this leads to reproductive suppression. Why do they not challenge the age convention? Perhaps because dominance carries physiological costs due to chronic GC elevation. To resolve these questions, data from more species on the association between GC levels and rank, together with data on the behavioral and demographic correlates of rank, are needed. To relate these patterns directly to fitness, research will have to be conducted in the wild; methods to measure steroid hormone levels with noninvasively collected urine and feces are in place for studies of this type (Box 3). Given the variability in observational studies of GCs and rank (Tables 1 and 2), experimental approaches are likely to be of great value. Opinion References 1 Wingfield, J.C. (1994) Modulation of the adrenocortical response to stress in birds. In Perspectives in Comparative Endocrinology (Davey, K.G. et al., eds), pp. 520–528, National Research Council 2 Sapolsky, R.M. (1992) Neuroendocrinology of the stress response. In Behavioral Endocrinology (Becker, J.B. et al., eds), pp. 287–324, Massachusetts Institute of Technology Press 3 Munck, A. et al. (1984) Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5, 25–44 4 Chrousos, G.P. and Gold, P.W. (1992) The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. J. Am. Med. Assoc. 267, 1244–1252 5 Pottinger, T.G. (1999) The impact of stress on animal reproductive activities. In Stress Physiology in Animals (Baum, P.H.M., ed.) pp. 130–177, CRC Press 6 Wingfield, J.C. and Ramenofsky, M. (1999) Hormones and the behavioral ecology of stress. In Stress Physiology in Animals (Baum, P.H.M., ed.) pp. 1–51, CRC Press 7 Buchanan, K.L. (2000) Stress and the evolution of condition-dependent signals. Trends Ecol. Evol. 15, 156–160 8 Astheimer, L.B. et al. (2000) Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea. Horm. Behav. 37, 31–39 9 Weiss, J. (1970) Somatic effects of predictable and unpredictable shock. Psychosom. Med. 32, 397–414 10 Louch, C.D. and Higginbotham, M. (1967) The relation between social rank and plasma corticosterone levels in mice. Gen. Comp. Endocrinol. 8, 441–444 11 Bronson, F.H. and Eleftheriou, B.E. (1964) Chronic physiological effects of fighting in mice. Gen. Comp. Endocrinol. 4, 9–14 12 Manogue, K.R. (1975) Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus). Primates 14, 457–463 13 Blanchard, D.C. et al. (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. 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(1992) Physiological and reproductive correlates of behavioural strategies in female domestic pigs. Anim. Behav. 44, 1107–1121 Articles of interest Articles of ecological or evolutionary interest in recent issues of other Trends and Current Opinion journals Host fecundity reduction: a strategy for damage limitation? Hilary Hurd Trends in Parasitology 17, 363–368 (August 2001) Signal and nutrient exchange at biotrophic plant–fungus interfaces, OC Yoder and B. Gillian Turgeon Current Opinion in Plant Biology 4, 315–321 (August 2001) Merging molecular and ecological approaches in plant–insect interactions, Ian T. Baldwin, Rayko Halitschke, Andre Kessler and Ursula Schittko Current Opinion in Plant Biology 4, 351–358 (August 2001)