Social mediation of sexually selected ornamentation and steroid hormone levels in male junglefowl

Honest signals in sexual selection may be maintained by a variety of mechanisms. Comb size in male red junglefowl, Gallus gallus, a well-known predictor of female mate choice, is mediated by health and condition. Social status has also been shown to mediate comb size. To determine whether hormones related to male dominance behaviour might be related to social status and comb size, we monitored changes in plasma levels of testosterone and corticosterone following manipulation of social status. We removed young adult male junglefowl from their all-male flocks and placed them either in individual cages or in smaller flocks. We measured comb size and other morphological variables, as well as testosterone and corticosterone levels, before and after the manipulation of social status. Males in small flocks showed reduced comb growth, increased corticosterone and decreased testosterone levels compared with individually housed males. Within flocks, comb size was positively related to dominance rank and to testosterone level, although not always significantly. However, dominance rank was unrelated to either corticosterone or testosterone levels. In isolated birds, testosterone level was not related to comb size. Corticosterone level was not related to comb size in either treatment group. Our results are consistent with social mediation of comb size and testosterone and corticosterone levels, but it is unclear whether these hormones contribute to the observed social limitation of comb length.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Sexual selection in gallus: Effects of morphology and dominance on female spatial behavior

Sexual selection has received a great deal of attention from field and laboratory researchers for over a century, but hard evidence of female choice of mates in mixed-sex groups remains scarce. Dominant males typically mate much more often than subordinants but evidence that females “choose” such males is elusive. In $\text{Gallus}$, which includes junglefowl and their domestic fowl descendants, females stay near and mate with dominant, territorial males. We demonstrate here that $\text{Gallus}$ females in mixed-sex flocks who have no information about the social dominance status of males orient to, approach and stay near males with larger than average combs whereas females which $\text{do}$ not have information about male dominance orient toward and stay near high ranking males. We verify that comb size correlates with male social rank. Hence, $\text{Gallus}$ females do actively respond to “high quality” males; they apparently identify such males by male physical characteristics and, if available, information concerning male-male interactions.     

The effects of previous experience and current condition on status contests in the bluebanded goby (<Emphasis Type="Italic">Lythrypnus dalli</Emphasis>)

Social status can change over a lifetime and affect fitness. Status transitions are often influenced by previous experience such that previous winners tend to dominate in future interactions, while losers tend to remain subordinate. We investigated the role of social status experience on future status contests in the bluebanded goby (Lythrypnus dalli), a highly social, sex-changing fish. Female L. dalli were given long-term experience as alpha (dominant) or beta (subordinate) in a stable social group of three fish (two females, one dominant male). We hypothesized that females with previous dominance experience would be more likely to become dominant in a novel context and change sex, a status-dependent transition. We found that in size-matched pairs, half of the previous alphas and half of the previous betas established and maintained dominance in the novel pair. Previous betas were more likely to become dominant in pairs with small relative differences in physical condition. Betas that initiated more interactions with the male in the stable group were also more likely to become dominant. Experience only had a transient effect on agonistic behavior during status establishment. In pairs in which the previous beta established dominance, individual agonistic efficiency, or the proportion of their approaches that led to a displacement, was lower. There was no long-term effect of experience on the rate of sex change. These data suggest that long-term tenure as a subordinate does not, itself, prevent status ascension and that physical condition and individual behavior are relevant factors that influence L. dalli contests.     

Playing chicken with red junglefowl: identifying phenotypic markers of genetic purity in Gallus gallus

We report the results of a novel experiment, in which genetically pure male red junglefowl Gallus gallus (Richardson strain) were deliberately crossed with domestic female chickens to create contaminated lines of known purity, reaching as high as 93.75%. Phenotypic characters generally used as indicators of purity (reduced or absent female comb, male eclipse plumage, etc.) all appeared to at least some extent in domestically contaminated progeny and moreso in successively more pure generations of the experiment, suggesting that such phenotypic characters may have little, if any, utility in characterizing red junglefowl stocks as to their genetic purity.     

Dynamic phenotypic correlates of social status and mating effort in male and female red junglefowl,Gallus gallus

Despite widespread evidence that mating and intrasexual competition are costly, relatively little is known about how these costs dynamically change male and female phenotypes. Here, we test multiple hypotheses addressing this question in replicate flocks of red junglefowl (Gallus gallus). First, we test the interrelationships between social status, comb size (a fleshy ornament) and body mass at the onset of a mating trial. While comb size covaried positively with body mass across individuals of both sexes, comb size was positively related to social status in females but not in males. Second, we test for changes within individuals in body mass and comb size throughout the mating trial. Both body mass and comb size declined at the end of a trial in both sexes, suggesting that mating effort and exposure to the opposite sex are generally costly. Males lost more body mass if they (a) were socially subordinate, (b) were chased by other males or (c) mated frequently, indicating that subordinate status and mating are independently costly. Conversely, females lost more body mass if they were exposed to a higher frequency of coerced matings, suggesting costs associated with male sexual harassment and female resistance, although costs of mating per se could not be completely ruled out. Neither competitive nor mating interactions predicted comb size change in either sex. Collectively, these results support the notion that sex‐specific costs associated with social status and mating effort result in differential, sex‐specific dynamics of phenotypic change.     

Social status in female bighorn sheep (Ovis canadensis): expression, development and reproductive correlates

Female bighorn sheep were studied over a 27-month period to quantify linearity and stability of social rank; expression of behaviour as a function of rank; development of rank relationships; and reproductive correlates of rank. Females exhibited a stable, non-linear hierarchy that correlated strongly with age. Dominant females used proportionally more threats, whereas subordinates used more subordinance patterns. Females integrated into the hierarchy at1–2 years of age and then fought their way to high social status. Dominant and subordinate females did not differ in pre-natal maternal investment, but dominant females nursed lambs at higher rates, and were more likely than subordinates to nurse alien lambs after their own lamb died.     

Social status does not predict corticosteroid levels in postdispersal male spotted hyenas

In social species with low rates of direct male competition levels of corticosteroids should not correlate with social status. Male spotted hyenas acquire social status by observing strict queuing conventions over many years, and thus levels of male-male aggression are low, and male social status and tenure are closely correlated. In this study, we investigated whether the low rate of direct male competition in spotted hyenas was reflected in fecal corticosteroid levels of adult males in the Serengeti National Park. Also, interactions with dominant females may influence corticosteroid levels of males, and it has been suggested recently that males with a long tenure (high rank) are more stressed by females than males with a short tenure (low rank). We tested whether there is a difference in the likelihood of being aggressively challenged by dominant females between long-tenured and short-tenured males. Short-tenured males were more likely to elicit an aggressive response by females than long-tenured males, but previous work suggests that they also interacted less frequently with females, thus avoiding putting themselves in a potentially stressful situation. Thus, as expected, the comparison of males in three different clans revealed no correlation between social status or tenure and fecal corticosteroid levels. However, males of the largest clan had the highest levels of fecal corticosteroids, possibly reflecting higher rates of social interactions in larger clans.     

Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus)

Abstract Females may choose more attractive mates to obtain better viability or attractiveness genes for their offspring. A number of studies have demonstrated a positive relationship between paternal attractiveness and offspring quality. However, this pattern could be due to inheritance of paternal genes and/or it could be due to increased maternal investment in the offspring of more attractive males. To isolate female responses to male appearance from paternal genetic effects, I housed female red junglefowl ( Gallus gallus ) with vasectomized (sterile) males and artificially inseminated them. Male junglefowl with larger combs are more attractive to females. Females laid more eggs when housed with a large-combed, as opposed to a small-combed, vasectomized mate. Neither egg volume nor offspring body condition was associated with comb size of the mother's vasectomized mate. Paternal genetics appeared important. Body condition and comb size were greater for the sons of large-combed sperm donor males. This is consistent with the hypothesis that genetic benefits to offspring maintain female preference for the most ornate males. It is possible that greater body condition and comb size in sons of large-combed sires was not caused by genetic differences, but instead was due to compounds in the ejaculate of large-combed sperm donors inducing greater reproductive investment from females. However, females artificially inseminated by large-combed males did not produce more or larger eggs than females artificially inseminated by small-combed males, and thus there is no other evidence consistent with ejaculate-induced differential investment. Furthermore, only in older chicks was body condition significantly related to sire comb size, suggesting genetic rather than differential investment mechanisms.     

Merging social hierarchies: Effects on dominance rank in male green swordtail fish (Xiphophorus helleri)

When the same set of individuals are placed in different social contexts, some groups members often experience a change in dominance status. We examined the context-dependence of social status using a group fusion protocol in male green swordtail fish (Xiphophorus helleri). Six individuals were matched for size and separated into two groups of three fish. Each triad established a stable hierarchy after which time the two subgroups were merged into one larger assemblage. The maintenance of within- and between-group rank relationships was examined. Relative rank was preserved within each subgroup across social contexts but we found no evidence that familiarity with dominant animals assists individuals of one subgroup in achieving higher rank (coat-tail effects). Dominant individuals from the pre-fusion groups were significantly likely to obtain high status in the merged group and vice versa for subordinate pre-fusion animals. These results demonstrate that social rank in swordtails is relatively impervious to changes in social context, but we address some deviations from this trend. Small differences in standard length were a significant predictor of the most dominant rank in the post-fusion hierarchy, with the largest animals tending to occupy the alpha position. We discuss our results in terms of the potential factors involved in within- and between-group rank maintenance, including individual recognition, winner and loser effects, or asymmetries in dominance-related characteristics.     

Male Reproductive Success in a Social Group of Urban Feral Cats (Felis catus L.)

Dominance rank, morphological characteristics and reproductive success of adult males were measured in a multi‐male multi‐female group of urban feral cats (Felis catus L.). Paternity of nine litters (34 kittens) of the domestic cat from six females was determined through microsatellites analyses at nine loci. The percentage of multiple paternities in this social group was as high as 78%. A positive correlation was found between male size/body weight and dominance. The males who sired the highest number of kittens were the dominant ones. Additionally, dominant males were more likely to be infected by the feline immunodeficiency virus, a virus transmitted by bites through aggressive interactions. Thus this study demonstrates that rank and body weight were both important in predicting the annual reproductive success. However, it shows that the reproductive benefit associated to rank may be balanced by cost due to at‐risk aggressive behaviour of dominant males.     

Multiple aspects of condition influence a heritable sexual trait: a synthesis of the evidence for capture of genetic variance in red junglefowl

A long‐standing question in the study of sexual selection is: if an attractive male trait signals heritable aspects of quality, how does genetic variation associated with that trait persist in the face of directional selection? It has been proposed that sensitivity to condition in general could allow a sexual signal to show heritable variation even under persistent directional selection. The multitude of genes underlying components of condition present a large target for mutation, and so genetic variance in condition may not be readily exhausted by selection. Insights gained in studies of the red junglefowl are relevant to this hypothesis, and provide a model for research in other systems. The fleshy comb of male red junglefowl is among the best‐studied sexual signals. Multiple components of condition, such as health, immune function, testosterone, and social status, influence comb growth, and, in the present study, we provide the first comprehensive integration of this large body of evidence to lay out the compelling case for condition‐dependence of the junglefowl comb. Variation in comb size is heritable and, most important to this issue, is genetically correlated with heritable variation in a body condition index. Although understanding of the red junglefowl's comb is far from complete, it exceeds our understanding of many other sexual signals and provides an empirical model for the study of condition‐dependent signals in general. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 651–660.     

Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx)

Subordinate female cercopithecine primates often experience decreased reproductive success in comparison with high-ranking females, with a later age at sexual maturity and first reproduction and/or longer interbirth intervals. One explanation that has traditionally been advanced to explain this is high levels of chronic social stress in subordinates, resulting from agonistic and aggressive interactions and leading to higher basal levels of glucocorticoids. We assessed the relationships among fecal cortisol levels and reproductive condition, dominance rank, degree of social support, and fertility in female mandrills (Mandrillus sphinx) living in a semi-free-ranging colony in Franceville, Gabon. Lower-ranking females in this colony have a reproductive disadvantage relative to higher-ranking females, and we were interested in determining whether this relationship between dominance rank and reproductive success is mediated through stress hormones. We analyzed 340 fecal samples from 19 females, collected over a 14-month period. We found that pregnant females experienced higher fecal cortisol levels than cycling or lactating females. This is similar to results for other primate species and is likely owing to increased metabolic demands and interactions between the hypothalamus-pituitary-adrenal axis, estrogen, and placental production of corticotrophin releasing hormones during pregnancy. There was no influence of dominance rank on fecal cortisol levels, suggesting that subordinate females do not suffer chronic stress. This may be because female mandrills have a stable social hierarchy, with low levels of aggression and high social support. However, we found no relationship between matriline size, as a measure of social support, and fecal cortisol levels. Subordinates may be able to avoid aggression from dominants in the large enclosure or may react only transiently to specific aggressive events, rather than continuously expecting them. Finally, we found no relationship between fecal cortisol levels and fertility. There was no difference in fecal cortisol levels between conceptive and nonconceptive cycles, and no significant relationship between fecal cortisol level and either the length of postpartum amenorrhea or the number of cycles before conception. This suggests that the influence of dominance rank on female reproductive success in this population is not mediated through chronic stress in subordinate females, and that alternative explanations of the relationship between social rank and reproduction should be sought.     

Sex-reversed correlation between stress levels and dominance rank in a captive non-breeder flock of crows

Group living has both benefits and costs to individuals; benefits include efficient acquisition of resources, and costs include stress from social conflicts among group members. Such social challenges result in hierarchical dominance ranking among group members as a solution to avoid escalating conflict that causes different levels of basal stress between individuals at different ranks. Stress-associated glucocorticoid (corticosterone in rodents and birds; CORT) levels are known to correlate with dominance rank in diverse taxa and to covary with various social factors, such as sex and dominance maintenance styles. Although there is much evidence for sex differences in the basal levels of CORT in various species, the correlation of sex differences in basal CORT with dominance rank is poorly understood. We investigated the correlation between CORT metabolites (CM) in the droppings and social factors, including rank and sex, in a captive non-breeder group of crows. In this group, all the single males dominated all the single females, and dominance ranks were stable among single males but relatively unstable among single females. CM levels and rank were significantly correlated in a sex-reversed fashion: males at higher rank (i.e., more dominant) had higher CM, whereas females at higher rank exhibited lower CM. This is the first evidence of sex-reversed patterns of CM–rank correlation in birds. The results suggest that different mechanisms of stress–dominance relationships operate on the sexes in non-breeder crow aggregations; in males, stress is associated with the cost of aggressive displays, whereas females experience subordination stress due to males' overt aggression.     

Correlates and Consequences of Dominance in a Social Rodent

In harem‐polygynous societies, body condition is often correlated with dominance rank. However, the consequences of dominance are less clear. High‐ranking males do not inevitably have the highest reproductive success, especially in systems where females mate with multiple males. In such societies, we expect male reproductive success to be more highly skewed than female reproductive success, but reproductive skew in females can still arise from rankings established within matrilineal societies. Dominance can also impact life‐history decisions by influencing dispersal patterns in yearlings. To better understand the function of dominance in harem‐polygynous societies, we studied the causes and consequences of dominance in yellow‐bellied marmots (Marmota flaviventris), a social rodent with skewed male reproductive success and female reproductive suppression. Specifically, we examined body condition as a predictor and the probability of breeding, number of offspring, and dispersal as outcomes of dominance. Additionally, we looked at variation in dominance between males and females and adults and yearlings, because marmots can engage in distinct interactions depending on the type of individuals involved. We found that marmots in better body condition have higher dominance rank than those in poorer condition. In addition, adults are dominant over yearlings. Within yearlings, dominance does not influence dispersal, but those in better body condition are less likely to disperse. Within all adults, individuals in better condition produce more offspring per year. Within adult males, more dominant males have greater reproductive success. Despite previous evidence of reproductive suppression in females, we found no effects of dominance rank on female reproductive success in the current study. The function of dominance in female marmots remains enigmatic.     

Social preferences of domestic hens for domestic vs. red junglefowl males and females

The striking dimorphism of male and female junglefowl may have evolved in large part due to female choice of mates. However, domestic fowl hens consistently chose domestic, not junglefowl, males as well as females in preference tests. Either genetic predisposition to favor junglefowl morphological features over those of the domestic types utilized in these tests was overridden by experience or such genetic predisposition does not exist in the breed we tested.     

Giving your daughters the edge: bequeathing reproductive dominance in a primitively social bee

The fitness associated with behavioural strategies is usually estimated in terms of offspring number and size. However, in group-living animals the reproductive value of offspring may also depend on their social rank. We show here that in an allodapine bee Exoneura robusta, dominant mothers can behaviourally influence their daughters'' reproductive rank by controlling insemination of other potential mothers. In E. robusta, group living is near mandatory and reproductive dominance among female nestmates is determined by order of adult emergence. Nests are single, undivided burrows and the dominant female assumes a guarding position closest to the nest entrance. We show that before the egg-laying period, subordinate females who have been absent from the nest are ''screened'' by the reproductive guard upon attempted re-entry. Those who have been in contact with foreign males are less likely to be granted access back into the nest than those who have been in contact with foreign females or with no bees at all. We argue that by controlling insemination patterns of their nestmates, dominant females ensure that their own daughters eclose first and are therefore more likely to assume dominance in the next generation. This presents a situation where dominance is bequeathed to daughters by behavioural means. The ability of mothers to influence social hierarchies in subsequent generations introduces a fitness component additional to the number and size of offspring produced.     

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

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

Quantitative genetics of sexually dimorphic traits and capture of genetic variance by a sexually-selected condition-dependent ornament in red junglefowl (Gallus gallus)

We studied the quantitative genetics of sexually selected traits in a captive population of red junglefowl (Gallus gallus L.) using a multi-generational 'animal model' approach. We found significant heritability of mass, tarsus length (both strongly sexually dimorphic), residual mass, and male comb (a fleshy head ornament) length. Residual mass has a genetic correlation between the sexes smaller than unity and so could show partially independent responses to selection in the two sexes. In males, tarsus length and mass were not genetically correlated, and this produced a negative genetic correlation between tarsus length and residual mass. The male red junglefowl's comb, an ornament influencing female choice, is highly condition dependent. We show that expression of this ornament is heritable, however, and shows strong genetic correlation with a condition index, residual mass. Because residual mass is partly influenced by various aspects of condition, it appears that comb size has 'captured' genetic variability in condition.     

Third-Party Ranks Knowledge in Wild Vervet Monkeys (Chlorocebus aethiops pygerythrus)

The Machiavellian/Social Intelligence Hypothesis proposes that a complex social environment selected for advanced cognitive abilities in vertebrates. In primates it has been proposed that sophisticated social strategies like obtaining suitable coalition partners are an important component of social intelligence. Knowing the rank relationships between group members is a basic requirement for the efficient use of coalitions and the anticipation of counter-coalitions. Experimental evidence for such knowledge currently exists in only few species. Here, we conducted rank reversal playback experiments on adult females belonging to three different groups of free-ranging vervet monkeys (Chlorocebus aethiops pygerythrus) to test their knowledge of the female hierarchy. Playbacks simulating rank reversals (subordinate aggressing a dominant) induced longer looking times than playbacks simulating a dominant aggressing a subordinate. Vervet monkey females therefore seem to compute the rank relationships between other females. Our results suggest that detailed social knowledge about rank relationships may be widespread in primates and potentially also in other species living in stable groups.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.