Female dominance in captive gray mouse lemurs (Microcebus murinus)

Female dominance or female feeding priority seem to be characteristic for many lemur species, but are rare traits in other primates and mammals in general. The nocturnal lemur species, however, are underrepresented in the quantitative studies on social dominance. The aim of this study is to investigate the pattern of intersexual dominance relationships in the gray mouse lemur (Microcebus murinus), a species that is generally thought to possess a number of ancestral lemur traits. The context, distribution, and outcome of intersexual conflicts are analyzed in four captive groups of gray mouse lemurs. Intersexual conflicts occurred in the study groups in different behavioral contexts and were mostly spatial interactions (chasing/fleeing, approach/avoidance). The majority of conflicts were decided, and were in all but one case won by females. This is the first evidence suggesting unconditional female dominance in a cheirogaleid primate. The existence of female dominance in most families of the Lemuriformes suggests it is an ancient trait that evolved in their common ancestor.     

Maintenance of female dominance in blue‐eyed black lemurs (Eulemur macaco flavifrons) and gray bamboo lemurs (Hapalemur griseus griseus) under semi‐free‐ranging and captive conditions

Several species of Malagasy prosimians are characterized by female dominance, an unusual trait among mammals. We compare the extent to which female dominance is displayed and the mechanisms that are used to maintain dominance in the frugivorous blue‐eyed black lemurs (Eulemur macaco flavifrons) and the folivorous gray bamboo lemurs (Hapalemur griseus griseus) housed at the Duke Lemur Center. All dominant–submissive interactions were recorded during 448 hr of focal animal observations. Both species of lemurs exhibited clear patterns of female dominance. However, the two species used aggressive dominance (defined as aggression+submission) and social dominance (defined as submission in the absence of aggression) to different extents in maintaining hierarchies within each group. The adult female blue‐eyed black lemurs used aggressive dominance (e.g., chase, cuff, bite) in more of their dominance interactions (66%) than did the adult female gray bamboo lemurs (40%). In both species, rates of aggressive dominance interactions were higher during feeding versus nonfeeding periods and while in smaller outdoor runs versus larger natural habitat enclosures, but the differences were not significant. Overall blue‐eyed black lemurs exhibit a more aggressive form of female dominance compared to the gray bamboo lemur. Zoo Biol 26:345–361, 2007. © 2007 Wiley‐Liss, Inc.     

Female dominance in blue-eyed black lemurs(Eulemur macaco flavifrons)

Female dominance is unusual among mammals and has been described in detail for only a handful of species. Here we present data on the frequency and outcome of dominance interactions in seven semi-free ranging and captive groups of blue-eyed black lemurs (Eulemur macaco flavifrons) housed at the Duke University Primate Center. We collected over 260 hours of focal data during which all occurrences of dominant-subordinate interactions were recorded. We collected data outside the typical breeding and birthing seasons for this species, thus eliminating possible confounding factors and increased aggression associated with these periods. We found that females were dominant over males in all seven groups, with females winning 99% of all dominance interactions.E. m. flavifrons used aggressive dominance (e.g. chase, cuff, bite) in 81% of all interactions, with the remainder of interactions being decided using social dominance (e.g. deference in the form of supplants or cowers). Older females were dominant over younger females in two out of three multi-female groups (in each case, younger females were daughters), and younger males (sons of the dominant female) received less aggression from females than did older males (n = 2 groups). Caging and group size appear to play a minimal role in the expression of female dominance. While confirmation must await further observations on free-ranging groups ofE. m. flavifrons, our data strongly suggest that this subspecies can be characterized as female dominant.     

Female social dominance in two Eulemur species with different social organizations

Female social dominance is rare in mammals, but common in lemurs. We investigated social dominance in two Eulemur species; the polygynous crowned lemur (E. coronatus) and the monogamous red‐bellied lemur (E. rubriventer), using four and two social groups, respectively. We collected data on agonistic interactions and two types of affiliative behavior (grooming and maintaining spatial proximity). We used a combination of focal watches of individuals, instantaneous scan‐sampling of groups, and all‐occurrence of some behaviors in groups. We found that overall rates of agonistic interactions were higher in E. coronatus, and they also had more decided intersexual agonistic interactions than E. rubriventer. However, in both species the females won the vast majority of these agonistic interactions. E. coronatus females were groomed more often by males than vice versa, whereas no sex differences in grooming were observed in E. rubriventer. We found that males were responsible for maintaining spatial proximity in E. coronatus whereas in E. rubriventer, females were responsible. In one group of E. coronatus, the male was overweight and dominant to the female and this is the first observation of male dominance in a lemur species typically described as female dominant. We suggest that body weights in captivity be monitored for maintaining normal dominance relationships. Overall, agonistic behaviors were consistent with clear female social dominance in both E. coronatus and E. rubriventer. The affiliative behaviors also provided clear evidence for female dominance E. coronatus, but not for E. rubriventer. Zoo Biol 0: 1–14, 2007. © 2007 Wiley‐Liss, Inc.     

Females competing to reproduce: dominance matters but testosterone may not

The associations among aggression, testosterone (T), and reproductive success have been well studied, particularly in male birds. In many species, males challenged with simulated or real territorial intrusions increase T and levels of aggression, outcomes linked to higher dominance status and greater reproductive success. For females, the patterns are less clear. Females behave aggressively towards one another, and in some species, females respond to a social challenge with increases in T, but in other species they do not. Prior work on female dark-eyed juncos (Junco hyemalis) had shown that experimental elevation of T increases social status and intrasexual aggression. Here, we conducted two experiments designed to answer three questions: Are endogenous concentrations of T associated with dominance status in captive female juncos? Does dominance status influence readiness to breed in female juncos? And do captive females increase T in response to a challenge? In the first experiment, we introduced two females to a breeding aviary, allowed them to form a dominance relationship and then introduced a male. We found that dominant females were more likely to breed than subordinates, but that dominance status was not predicted by circulating T. In the second experiment, we allowed a resident male and female to establish ownership of a breeding aviary (territory) then introduced a second, intruder female. We found that resident females were aggressive towards and dominant over intruders, but T did not increase during aggressive interactions. We suggest that during the breeding season, intrasexual aggression between females may influence reproductive success, but not be dependent upon fluctuations in T. Selection may have favored independence of aggression from T because high concentrations of T could interfere with normal ovulation or produce detrimental maternal effects.     

Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally 'masculinized'?

Female social dominance characterizes many strepsirrhine primates endemic to Madagascar, but currently there is no comprehensive explanation for how or why female lemurs routinely dominate males. Reconstructing the evolutionary pressures that may have shaped female dominance depends on better understanding the mechanism of inheritance, variation in trait expression, and correlating variables. Indeed, relative to males, many female lemurs also display delayed puberty, size monomorphism, and 'masculinized' external genitalia. As in the spotted hyena (Crocuta crocuta), a species characterized by extreme masculinization of the female, this array of traits focuses attention on the role of androgens in female development. Consequently, I examined endocrine profiles and social interaction in the ringtailed lemur (Lemur catta) to search for a potential source of circulating androgen in adult females and an endocrine correlate of female dominance or its proxy, aggression. I measured serum androstenedione (A(4)), testosterone (T), and estradiol (E(2)) in reproductively intact, adult lemurs (10 females; 12 males) over four annual cycles. Whereas T concentrations in males far exceeded those in females, A(4) concentrations were only slightly greater in males than in females. In both sexes, A(4) and T were positively correlated, implicating the Delta(4)-biosynthetic pathway. Moreover, seasonal changes in reproductive function in both sexes coincided with seasonal changes in behavior, with A(4) and T in males versus A(4) and E(2) in females increasing during periods marked by heightened aggression. Therefore, A(4) and/or E(2) may be potentially important steroidal sources in female lemurs that could modulate aggression and underlie a suite of masculinized features.     

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.     

Social Network Analysis of Male Dominance in the Paper Wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Social aggression is a pervasive feature of insect societies. In eusocial Hymenoptera, aggression among females can affect task performance and competition over direct reproduction (egg laying); in most species males participate in social interactions relatively rarely. Males of the independent-founding paper wasp Mischocyttarus mastigophorus are exceptional: they are aggressive toward female nestmates, leading us to explore the function of this unusual behavior. We applied social network analyses to data on M. mastigophorus social aggression to quantify sex differences in giving and receiving social aggression. The network analyses supported the pattern of biased male aggression toward female nestmates; females are relatively rarely aggressive to males. We then asked whether male aggression toward females was biased by females’ relative ovary development. Males were more aggressive toward females with better-developed ovaries, opposite to patterns of aggression among females. Because food brought to the colonies is often monopolized by dominant females, we suggest that males direct aggression toward socially dominant females with better-developed ovaries to obtain food. The implications of biased male aggression for female task performance and physiology are unknown.

     

Female aggression in red deer: Does it indicate competition for mates?

Female–female competition over mates is often considered of minor importance, particularly in polygynous species. In red deer (Cervus elaphus), female–female aggression within harems during the breeding season has not been studied to date. Herein, we examined if oestrous female red deer in harems show elevated aggression rates, compared to when they are in harems but not in oestrous, and also when they are in foraging groups outside of the breeding season. Any increased levels of aggression involving oestrous females, could indicate the potential for female–female competition for mates in this species. We found that aggressive interactions among female red deer were clearly evident. The most common forms of aggression were displacements, nose threats and kicking. Biting and ear threats occurred less frequently, and chases were rare. There were no differences in the proportion of the different aggression types in the three social contexts. More importantly, we found that the highest overall rates of aggression were for oestrous females in harems, and for females in foraging groups. The lowest rates of aggression were found in harems (when the focal female was not in oestrous). If high rates of aggression also occur when several females are simultaneously in oestrous within single harems, then it is possible that this aggression could affect either mate choice or mating order. These results suggest that female–female competition over mates could play a role in the mating behaviour of red deer.     

Context matters: female aggression and testosterone in a year-round territorial neotropical songbird (Thryothorus leucotis)

Testosterone promotes aggressive behaviour in male vertebrates during the breeding season, but the importance of testosterone in female aggression remains unclear. Testosterone has both beneficial and detrimental effects on behaviour and physiology, prompting the hypothesis that selection favours an association between aggression and testosterone only in certain contexts in which intense or persistent aggression may be beneficial. We tested this hypothesis in a year-round territorial female buff-breasted wrens (Thryothorus leucotis), by exposing free-living females to experimental intrusions in different social (either single female or male, or paired decoys) and seasonal (pre-breeding or breeding) contexts. Females responded more aggressively to intrusions by females and pairs than to males. However, female intrusions elicited stronger responses during pre-breeding, whereas responses to pair intrusions were more intense during breeding. Territorial females had elevated testosterone levels after female intrusions and intermediate levels after pair intrusions during pre-breeding, but the levels of testosterone remained low after these intrusions during breeding. These results demonstrate seasonal differences in circulating testosterone following territorial aggression in female buff-breasted wrens and are suggestive of differences according to social context as well. Context-dependent elevation of testosterone implies that selection acts directly on female vertebrates to shape patterns of testosterone secretion.     

Virgin females compete for mates in the male lekking species Ceratitis capitata

Abstract. Aggressive behaviour occurring in intrasexual competition is an important trait for animal fitness. Although female intrasexual aggression is reported in several insect species, little is known about female competition and aggressive interactions in polygynous male lekking species. The interactions of female Mediterranean fruit flies, Ceratitis capitata (a male lekking species), with other females and mating pairs under laboratory conditions are investigated. Mature, unmated (virgin) females are aggressive against each other and against mating pairs, whereas immature females are not. Female aggression against other females decreases dramatically after mating; however, mated females maintain aggression against mating pairs. In addition, higher intrasexual aggression rates are observed for mature, virgin females than for virgin males of the same age. The results show that female aggressiveness is virginity related, suggesting female competition for mates. These findings have important implications for understanding the physiological aspects of a complex social behaviour such as aggression and should stimulate further research on female agonistic behaviour in male lekking mating systems.     

Dominance,Age and Aggression among Female Pronghorn,Antilocapra americana (Family: Antilocapridae)

The relationships among dominance, age and aggressive behaviour of marked, female pronghorn (Antilocapra americana; Family Antilocapridae) were studied in north central Colorado. Females formed dominance hierarchies with few circular relationships. Unlike other female ungulates, dominance rank was not correlated with age. Dominance rank was negatively correlated with rate of aggression initiated in summer and winter; however, aggressiveness as an individual trait was not related to dominance. Older females received higher rates of aggression than younger females in summer and winter. During the rut, dominance rank was correlated with rate of aggression received but not with rate of aggression initiated. Patterns of aggression that differ by season within a given hierarchy of dominance relationships suggest a different cause or function of aggressive behaviour in different seasons.     

You are Not Welcome: Social Exchanges between Female Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Group living leads to competition for food between group members. Two types of intragroup food competition may occur: scramble competition, in which all group members use the same resource, such that feeding opportunities are equal for everyone; and contest competition, in which some group members monopolize resources through aggression and dominance. In species in which females disperse from the natal group and immigrate into other groups, immigrant females increase group size and thus possibly food competition. Under these circumstances, other females may use aggression to discourage new females from joining the group. We assessed the distribution of aggression, embraces, and kisses among female spider monkeys (Ateles geoffroyi) in relation to group tenure. We recorded social interactions during 1688 10-min focal animal samples on 11 females in Santa Rosa, Costa Rica. We found that aggression was rare between long-term resident females and aggression rates were not higher during feeding than in other contexts, suggesting there was little contest competition. Long-term residents and less recently immigrant females showed higher aggression rates toward the most recent immigrants than toward other females, especially during the first months after a female immigrated, which coincided with the dry season. We did not find similar patterns for embrace and kiss. These results suggest that other females target aggression toward the most recent immigrants to reduce scramble competition. This finding suggests that group tenure should be included in socioecological models for species with female dispersal.     

Social interactions among female rhesus macaques (Macaca mulatta) during the nonbreeding season: Responses to the introduction of males

When rhesus monkeys are observed in social groups during the breeding season, increases in interfemale aggression coincide with midcycle increases in sexual activity between males and females. However, some investigators have suggested that both aggressive and affiliative interactions between females are influenced by the presence or absence of males, irrespective of menstrual cycle stage. In the present study, social interactions among members of a captive group of rhesus females were measured during the non-breeding season in response to the introduction of rhesus males. Ovariectomized rhesus females (estrogen-treated or untreated) served as stimulus controls. Tests with males were characterized by significantly decreased interfemale proximity and grooming and significantly increased aggression from that seen in tests with stimulus females or in the absence of stimulus animals. Only interfemale proximity declined significantly during stimulus female tests, but results suggest that this may merely reflect a decline in this behavior that occurs across the course of the day. Estrogen treatment did not alter either the aggressive or affiliative behavior of stimulus females or group female response to stimulus females. The possibility is discussed that changes in interfemale interactions during tests with males reflect female interest in interacting with the male, particularly under social conditions that may limit such interactions.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Androgens and the role of female "hyperaggressiveness" in spotted hyenas (Crocuta crocuta)

It has been suggested that female dominance in spotted hyenas evolved due to selection for "hyperaggressive" androgenized females. According to this view, virilized external genitalia of female hyenas developed as a byproduct of selection for "androgen-facilitated social dominance." The evidence that female hyenas have higher androgen levels than males or other female mammals is inconclusive. We compared concentrations of testosterone (T), 5alpha-dihydrotestosterone (DHT), and androstenedione (AE) from a population in the Serengeti. Females had significantly lower T and DHT levels than predispersal and postdispersal males. AE levels did not significantly differ between females and postdispersal males, but were significantly lower in predispersal males. Our results, and those from studies that have demonstrated that male and female hyenas experience similar levels of maternal androgens during fetal development, provide little support for a theory of selection for female dominance and hyperaggressiveness through enhanced secretion of androgens. Our data are consistent with an alternative view that female virilization is a byproduct of selection for precocial aggressive cubs of both sexes. According to this view, high investment in lactation favored selection for accelerated fetal development, high neonatal aggression, and facultative siblicide.     

Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates

The goals of this study were to analyze the origin and function of sex differences in the size of canine teeth among Malagasy lemurs and other strepsirhine primates. These analyses allowed me to illuminate interactions between different mechanisms of sexual selection and to elucidate constraints on this sexually-selected trait. In contrast to central predictions of sexual selection theory, polygynous lemurs lack both sexual dimorphism in body size and male social dominance, but the degree of sexual dimorphism in the size of their canines is not known. A comparison of male and female canine size in 31 species of lemurs and lorises revealed significant male-biased canine dimorphism in only 6 of 13 polygynous lemur species. This result is in contrast to predictions of a hypothesis that would explain the lack of size dimorphism in lemurs as a result of high viability costs because canine teeth presumably have low maintenance costs and because they are used as weapons in male-male combat. Moreover, because females had significantly larger maxillary canines than males in only one lemur species, female dominance is not generally based on female physical superiority and selective forces favoring female dominance do not constrain sexual canine dimorphism in the sense of a pleiotropic effect. Contrary to predictions of sexual selection theory, species differences in canine dimorphism across strepsirhines were neither associated with differences in mating system, nor with the potential frequency of aggression. Variation in canine dimorphism was also unrelated to differences in body size, but there were significant differences among families, pointing to strong phylogenetic constraints. This study demonstrated that polygynous lemurs are at most subject to weak intrasexual selection on dental traits used in male combat and that traits thought to be under intense sexual selection are strongly influenced by phylogenetic factors.     

Social influences on plasma testosterone levels in male talapoin monkeys

Three social groups of laboratory-housed talapoin monkeys (Miopithecus talapoin) consisting of four adult males and four or five adult females, were observed over a 4-year period. All females were ovariectomized and given estradiol implants at intervals to render them sexually attractive; except for two castrated males with testosterone implants, all males were intact. Sexual and aggressive interactions were recorded, and testosterone levels were measured in plasma taken from males twice weekly. In each group males formed a linear dominance order, defined in terms of the direction of aggression between animals. The hormonal responses of intact males were monitored with respect to the presence of attractive females, access to these females, and transfer from the social group to isolation. In all groups the behavioral and endocrine responses of males to these treatments were rank related. In some instances, rising in rank was associated with elevated testosterone and falling in rank with decreased testosterone; these hormonal changes were associated with changes in sexual and aggressive interactions. The effects of sexual and aggressive behavior on plasma testosterone titers are discussed.     

Sex of opponent influences response to a potential status signal in house sparrows

We evaluated the possible use of a sexually dimorphic plumage trait as a status signal in inter- and intrasexual social interactions in free-living house sparrows, Passer domesticus. Males with larger black throat patches (bibs) tended to be dominant regardless of the opponent's sex. This relationship was maintained after controlling for body size and age in multivariate analyses. However, the nature of social interactions varied according to the sex of the opponent and a male's bib size. Males with larger bibs tended to be less aggressive to male opponents, and received significantly less aggression from those birds, a key predicted benefit of a status signal. However, when the opponent was a female, males with large bibs displayed significantly more aggression than males with small bibs, and this relationship persisted even after controlling for the dominance status of the participants. Females were significantly more aggressive towards male opponents than towards female opponents, and females interacting with two males of known bib size were more aggressive to the one with the larger bib. These results suggest that the bib of male house sparrows may be a signal of status, but that in interactions with females, the bib may also have other functions. Frequent testing by females of the underlying quality being signalled by the bib may be linked to later mate choice, and might be adaptive if the information value of the bib varies among years. Such testing may also contribute to mechanisms for maintaining the bib as a reliable signal of status. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Sex-specific interactions between aggressive and sexual behavior in the rat: Effects of testosterone and progesterone

The influence of progesterone on sexual and aggressive behaviors during aggressive encounters was investigated in pairs of TP-treated male and female rats. Gonadectomized females, chronically injected with testosterone propionate (TP), showed low but consistent levels of feminine sexual behavior which alternated with aggression. Progesterone when given in addition to TP facilitated receptive and proceptive behaviors, but reduced levels of aggression. In TP-treated males, levels of aggression were the same as observed in TP-treated females. However, TP-treated males seldomly showed sexual behavior during aggressive encounters and additional treatment with progesterone did not affect their behavior. After the aggression tests, animals were tested in a social preference test in which an ovariectomized female cage mate and the opponent from the aggressive encounter served as incentives. Positive correlations between levels of aggression and social preference for an opponent were found in both sexes, although correlations only reached statistical significance when progesterone was given in addition to TP. These correlations were found in both sexes, despite the fact that group analysis revealed pronounced sex differences in social preference: males preferred to spend their time near ovariectomized female cage mates, whereas females divided their time equally among female cage mates and opponents.