Integrating the female masculinization and challenge hypotheses: Female dominance, male deference, and seasonal hormone fluctuations in adult blue-eyed black lemurs (Eulemur flavifrons).

In the decades since female social dominance was first described in strepsirrhine primates, researchers have sought to uncover the proximate and ultimate explanations for its development. In the females of various female-dominant species, androgens have been implicated as regulators of behavior and/or predictors of seasonal fluctuations in aggression (the 'Female Masculinization Hypothesis'). Males, more generally, respond to changing social demands via seasonal fluctuations in androgen-mediated behavior (the 'Challenge Hypothesis'), that may also entail changes in activation of the hypothalamic-pituitary-adrenal axis. Here, we explore if androgens, glucocorticoids, and intersexual behavior fluctuate seasonally in the female-dominant, blue-eyed black lemur (Eulemur flavifrons), with potential consequences for understanding female aggression and male deference. Across two studies conducted during the breeding and nonbreeding seasons, we assessed rates of mixed-sex, dyadic social behavior (aggression and affiliation) and concentrations of fecal glucocorticoid metabolites (Study 1) and serum sex hormones (androstenedione, testosterone, and estradiol; Study 2). Our results align with several predictions inspired by the Female Masculinization and Challenge Hypotheses for intersexual relations: During the breeding season, specifically, both aggression and androstenedione peaked in females, while female-initiated affiliation decreased, potentially to facilitate female resource access and reproductive control. By comparison, all target hormones (androgens, estrogen, and glucocorticoids) peaked in males, with glucocorticoid concentrations potentially increasing in response to the surge in female aggression, and unusually high estrogen concentrations year-round potentially facilitating male deference via male-initiated affiliation. These results suggest complex, seasonally and hormonally mediated behavior in Eulemur flavifrons.

Food availability and male deference in the female-dominant ring-tailed lemur, Lemur catta.

Female dominance, a trait common to some Malagasy lemurs, has been viewed as an adaptation that decreases intersexual feeding competition. A hypothesized relationship exists between male "deference" (male submission in the absence of female aggression) and food availability. Sauther (1993) suggested that male ring-tailed lemurs at the Duke Lemur Center (Pereira et al., 1990) show more deference to females than do males in the wild owing to food abundance in captivity. To reexamine the link between food availability and male deference, we studied agonism and foraging in two nonwild ring-tailed lemur (Lemur catta) populations: the Los Angeles Zoo and St. Catherines Island (SCI). On SCI, we collected data under two feeding conditions: Low Provisions (low food availability) and High Provisions (high food availability). As expected, male deference measures at our study sites were more similar to measures of deference from other studies of L. catta in captivity than in the wild. Additionally, the change at SCI from low to high food availability was associated with increased male deference to females. Interestingly, male proximity to females during foraging at this location did not notably change between the low to high food availability conditions, suggesting that males were food competitors of females just as often under both feeding conditions. The increase in male deference under conditions of high food availability on SCI was due to males withdrawing more rapidly from female approaches during agonistic interactions. Hence, where food is more abundant, male L. catta are more likely to show submission to females, which appears to be a self-serving means of avoiding female aggression. Lemur males who are well-fed appear less apt to risk female aggression to obtain resources than more nutritionally stressed males. Our results support the view of female dominance in lemurs as an adaptive evolutionary response to conditions of resource limitation.

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

BACKGROUND: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear.The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. RESULTS: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. CONCLUSION: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

Exploring Social Dominance in Wild Diademed Sifakas (Propithecus diadema): Females Are Dominant, but It Is Subtle and the Benefits Are Not Clear.

Rarely observed in mammals, female dominance is documented in several of Madagascar's lemurs. Although dominance affects many aspects of primates' lives, studies have largely focused on dyadic agonistic interactions to characterise relationships. We explored the power structure of three diademed sifaka groups (Propithecus diadema) at Tsinjoarivo during the lean season (July-August, 325 h) using social behaviours, group leadership, displacements and feeding outcomes. Two groups had a hierarchy dominated by the breeding female, while the highest rank was held by the breeding male in the third; in dyadic interactions, breeding females dominated males in all groups. Inconsistencies in hierarchies suggest that groups vary, with rank related to kinship ties of breeders. Aggression and grooming were rare; adult females received aggression at lower frequencies than males. Group movements were led more by females and followed more by males, and female feeding priority was evident in displacements during feeding. However, males and females did not differ in feeding outcomes, as expected (particularly in the lean season) if female dominance (and/or male deference) serves to ensure better access for females. This unexpected pattern (female dominance despite rare aggression, clear female leadership and displacement, yet no observable benefit in grooming or feeding outcomes) defies easy explanation, and reinforces the fact that studies examining female power in lemurs should take a multifaceted approach. Further study is needed to understand this pattern, the physiological and reproductive consequences of female dominance (e.g. detecting subtler variation in food quality or intake rates) and exactly how (and when) the benefits of female dominance are manifested.

Expression of endogenous phospholipase D1, localized in mouse submandibular gland, is greater in females and is suppressed by testosterone.

To clarify the signal transduction mechanism in the differentiation and secretion of salivary glandular cells, the present study was attempted to examine in the submandibular gland (SMG) of mice, the expression and localization of phospholipase D1 (PLD1), one of the important effector molecules working in response to the activation of intramembranous receptors by first messengers. In immunoblotting analysis, the expression of PLD1 was high at postnatal 4 weeks (P4W) and decreased at P8W, and it was at negligible levels at newborn stage (P0W) and postnatal 2 weeks (P2W). The expression of PLD1 was greater in females, and it was suppressed by administration of testosterone to female mice. In immuno-light microscopy, immunoreactivity for PLD1 at P4W was moderate to intense, in the forms of dots and globules mainly in the apical domains of immature granular convoluted tubule (GCT)-cells localized largely in the proximal portion of the female GCT. By P8W, it decreased in intensity and remained weak to moderate along the apical plasmalemma of cells throughout the course of the female GCT, whereas it was faint throughout the GCT of the male SMG at P4W and negligible at P8W. In immuno-electron microscopy, immature GCT-cells characterized by electron-lucent granules were immunoreactive and the immunoreactive materials were deposited close to, but not within, those granules. Typical GCT cells, characterized by electron-dense granules, were immunonegative. No significant immunoreaction for PLD1 was seen in acini of SMGs of either sex at any time point examined. It is suggested that PLD1 is involved in the signaling for secretion of immature GCT cells and influences differentiation of these cells, probably through their own secretory substances.

Organizational and activational androgens, lemur social play, and the ontogeny of female dominance.

The role of androgens in shaping "masculine" traits in males is a core focus in behavioral endocrinology, but relatively little is known about an androgenic role in female aggression and social dominance. In mammalian models of female dominance, including the ring-tailed lemur (Lemur catta), links to androgens in adulthood are variable. We studied the development of ring-tailed lemurs to address the behavioral basis and ontogenetic mechanisms of female dominance. We measured behavior and serum androgen concentrations in 24 lemurs (8 males, 16 females) from infancy to early adulthood, and assessed their 'prenatal' androgen milieu using serum samples obtained from their mothers during gestation. Because logistical constraints limited the frequency of infant blood sampling, we accounted for asynchrony between behavioral and postnatal hormone measurements via imputation procedures. Imputation was unnecessary for prenatal hormone measurements. The typical sex difference in androgen concentrations in young lemurs was consistent with adult conspecifics and most other mammals; however, we found no significant sex differences in rough-and-tumble play. Female (but not male) aggression increased beginning at approximately 15 months, coincident with female puberty. In our analyses relating sexually differentiated behavior to androgens, we found no relationship with activational hormones, but several significant relationships with organizational hormones. Notably, associations of prenatal androstenedione and testosterone with behavior were differentiated, both by offspring sex and by type of behavior within offspring sexes. We discuss the importance of considering (1) missing data in behavioral endocrinology research, and (2) organizational androgens other than testosterone in studies of female dominance.

Sources of variation in social tolerance in mouse lemurs (Microcebus spp.).

BACKGROUND: Social tolerance strongly influences the patterns of affiliation and aggression in animal societies. However, not much is known about the variation of social tolerance in species living in dispersed social systems that combine solitary foraging activities with the need of coordinating social interactions with conspecifics on a regular basis. This study aims to investigate the sources of variation in social tolerance within a Malagasy primate radiation with dispersed social systems, the mouse lemurs (Microcebus spp.). Six mouse lemur species were selected as model species that belong to three different taxonomic clades, live in two types of forest environments (dry and humid), and differed in this study with respect to their reproductive activity. Six male-female and six male-male dyads of each species were tested temporarily in a standardized social encounter paradigm in Madagascar to collect data on joint use of space, non-agonistic body contacts, aggression rates, the number of conflicts and the establishment of intra- and intersexual dominance. RESULTS: Male-female dyads of the six species differed significantly in the frequency of affiliative and agonistic behaviors. In contrast, the variations between male-male dyads could not be explained by one parameter only, but clade membership, forest type, reproductive state as well as species were all suggested to be partially influential. Only one species (Microcebus mamiratra) showed signals of unambiguous female dominance in all male-female dyads, whereas the others had no or only a few dyads with female dominance. CONCLUSIONS: Variations in social tolerance and its consequences are most likely influenced by two factors, ecology (via forest type) and physiology (via reproductive activity), and only to a lesser extent by clade membership. The study suggests that mouse lemur females have higher aggression rates and more agonistic conflicts with males when females in the population are reproducing, at least in resource-rich humid forests. The study confirms a high degree of social plasticity between species in these small solitary foragers that supports their taxonomic distinctiveness and requires further scientific attention.

Reproductive endocrine patterns and volatile urinary compounds of Arctictis binturong: discovering why bearcats smell like popcorn.

Members of the order Carnivora rely on urinary scent signaling, particularly for communicating about reproductive parameters. Here, we describe reproductive endocrine patterns in relation to urinary olfactory cues in a vulnerable and relatively unknown viverrid--the binturong (Arctictis binturong). Female binturongs are larger than and dominate males, and both sexes engage in glandular and urinary scent marking. Using a large (n = 33), captive population, we collected serum samples to measure circulating sex steroids via enzyme immunoassay and urine samples to assay volatile chemicals via gas chromatography-mass spectrometry. Male binturongs had expectedly greater androgen concentrations than did females but, more unusually, had equal estrogen concentrations, which may be linked to male deference. Males also expressed a significantly richer array of volatile chemical compounds than did females. A subset of these volatile chemicals resisted decay at ambient temperatures, potentially indicating their importance as long-lasting semiochemicals. Among these compounds was 2-acetyl-1-pyrroline (2-AP), which is typically produced at high temperatures by the Maillard reaction and is likely to be responsible for the binturong's characteristic popcorn aroma. 2-AP, the only compound expressed by all of the subjects, was found in greater abundance in males than females and was significantly and positively related to circulating androstenedione concentrations in both sexes. This unusual compound may have a more significant role in mammalian semiochemistry than previously appreciated. Based on these novel data, we suggest that hormonal action and potentially complex chemical reactions mediate communication of the binturong's signature scent and convey information about sex and reproductive state.

A comparison of activity patterns for captive Propithecus tattersalli and Propithecus coquereli.

The activity patterns and social interactions of two species of captive sifaka were observed during a 2-year period. Allogrooming was not observed in golden-crowned sifaka and they spent significantly more time resting than the Coquerel's sifaka. Females of both species were found to be dominant to males. The golden-crowned sifaka (Propithecus tattersalli) spent significantly less time feeding than the Coquerel's sifaka. Temperature, time of day, species, and interpair comparisons for the golden-crowned sifaka were found to affect activity and social interactions, while gender did not. Like the Coquerel's sifaka, the golden-crowned sifaka was found to be diurnal; however, they differed in that the golden-crowned sifaka did not descend to the ground.

Shades of gray mouse lemurs: Ontogeny of female dominance and dominance-related behaviors in a nocturnal primate.

The ontogeny and establishment of dominance relationships in young individuals have been investigated in various group-living, diurnal primates but respective information is almost entirely lacking for nocturnal, non-gregarious species. As in many other mammals male primates often represent the dominant sex, but the opposite phenomenon (female dominance) is particularly frequent in lemurs, although almost nothing is known about its development. Therefore, we investigated the development of intersexual dominance in parallel to age-related changes in other relevant behaviors in the gray mouse lemur, a solitary forager with female dominance. In particular, the temporal trajectories of social play, marking behavior, social tolerance, and agonistic behaviors were characterized in captive dyads of three different age categories (ACs), among juveniles (ACI: 4-5 months, N = 6), adolescents (ACII: 8-9 months, N = 8) and young adults (ACIII: 12-13 months, N = 8). Data were collected during a series of three encounter experiments between one male and one female per dyad and age category (total observation time: 49.5 hr). Play behavior was observed in all age classes, although the number of playing dyads decreased with increasing age. A significant age-dependent increase in marking behavior was found in females, especially in substrate rubbing and urine washing, but not in males. Although conflict rates did not differ significantly between ACs, females started to win more conflicts from ACII onwards, and social tolerance decreased partly with increasing age. Clear dominance relationships were not observed in ACI and first indications of dominant females were found in ACII with an increasing number in ACIII. This study provides first information about the ontogeny of female dominance in a nocturnal primate and shows that this behavior develops relatively late during ontogeny. In conclusion, this study provides evidence for significant changes in the social lives of maturing mouse lemurs and a rather late social maturation in this species.

Reasons why women are more likely to develop primary biliary cholangitis.

Primary biliary cholangitis (PBC) is a chronic autoimmune disease of biliary stasis in which immune factors cause the gradual destruction of small bile ducts, biliary stasis, and eventually the development of liver fibrosis, cirrhosis, and even liver failure. One of the main characteristics of PBC is that it primarily affects middle-aged women, but the precise cause is still unknown. This article analyzes the unique causes and mechanisms of the female predominance of PBC and summarizes the potential causes.The female domination of PBC is reported to be primarily caused by sex hormones, environmental circumstances, and epigenetic changes, each of which has a different subtle impact on patients' gender disparities.

Pollinator Diversity and Phenological Interplay: Exploring Mineral, Hormonal, Sugar, and Vitamin Contents in Vitis vinifera L. cv Bozcaada Çavusu.

Unraveling the intricate physiological and biochemical intricacies associated with female dominance in grape berries across diverse developmental stages is imperative for optimizing grape production and ensuring the attainment of high-quality yields. This study conducted a thorough analysis of grape berries across phenological stages (BBCH-79, BBCH-81, BBCH-89) and cultivars. At BBCH-89, Bozcaada Çavusu*Vasilâki demonstrated the highest berry weight and total soluble solids (TSS) levels, emphasizing its enological potential. Acidity peaked at BBCH-79 (28.16) and declined at BBCH-89 (6.11), signaling a shift towards lower acidity in later stages. Bozcaada Çavusu*Vasilâki consistently showed the highest maturity index (MI). Mineral content variations were observed across nitrogen (N), calcium (Ca), potassium (K), phosphorus (P), magnesium (Mg), sulfur (S), iron (Fe), manganese (Mn), boron (B), zinc (Zn), and copper (Cu), with Bozcaada Çavusu*Vasilâki often having the highest concentrations, particularly in potassium, calcium, and boron. Hormonal analysis revealed a significant surge in concentrations at BBCH-89, with Bozcaada Çavusu*Vasilâki standing out. Notably, Indole-3-acetic acid (IAA) concentrations increased by 106%, and abscisic acid (ABA) levels peaked at BBCH-79 with a 38% increase in Bozcaada Çavusu*Kuntra. Sugar content analysis showed variations in fructose, glucose, sucrose, rhamnose, xylose, galactose, and arabinose levels across sampling times and cultivars. Bozcaada Çavusu*Vasilâki consistently exhibited higher sugar levels, especially at BBCH-81 and BBCH-89. Vitamin concentrations varied temporally and among cultivars, with BBCH-89 displaying the highest vitamin A concentration (6.24 mg/100 g FW), and Bozcaada Çavusu*Vasilâki often exhibiting maximum values for vitamin B1, B2, B6, and C. Further research and targeted cultivation practices focusing on the unique attributes of Bozcaada Çavusu*Vasilâki could enhance grape production efficiency, emphasizing its potential contribution to achieving consistently high-quality yields across various phenological stages.

Evolutionary Patterns of Intersexual Power.

Dominance and leverage are both possible causes of social inequality. If sexual dimorphism influences patterns of intersexual dominance, we predicted that highly dimorphic species are constrained to exhibit male-biased power (MP), but species with low sexual dimorphism are free to demonstrate a broader range of intersexual power relationships. If market effects influence intersexual leverage, we predicted that females have more power when group composition is more male-biased and estrus is asynchronous. We analyzed data on intersexual power, sexual dimorphism, expected estrous overlap, and sex ratio for 79 extant primate species using phylogenetic logistic regression and ancestral state reconstructions. Although MP is more common, every major primate clade includes non-MP species. MP was associated with greater body mass and canine length dimorphism and with female-biased sex-ratios. Low estrous overlap was associated with non-MP. Although MP was reconstructed as likely ancestral for anthropoids, the last common ancestor of this clade probably did not exhibit high sexual dimorphism. The last common ancestor of catarrhines was probably highly dimorphic, potentially constraining intersexual power relationships. Non-MP probably evolved multiple times in primates and may be less common because multiple traits are linked to MP while fewer traits are associated with female-biased power or equality.

Corrigendum: Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys.

[This corrects the article DOI: 10.3389/fpsyg.2020.00839.].

Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys.

Intersexual dominance relations are important for female mammals, because of their consequences for accessing food and for the degree of sexual control females experience from males. Female mammals are usually considered to rank below males in the dominance hierarchy, because of their typical physical inferiority. Yet, in some groups or species, females are nonetheless dominant over some males (partial female dominance). Intersexual dominance, therefore, also depends on traits other than sexual dimorphism, such as social support, social exchange, group adult sex-ratio, and the widespread self-reinforcing effects of winning and losing fights, the "winner-loser effect." The importance of sex-ratio and the winner-loser effect remains poorly understood. A theoretical model, DomWorld, predicts that in groups with a higher proportion of males, females are dominant over more males when aggression is fierce (not mild). The model is based on a small number of general processes in mammals, such as grouping, aggression, the winner-loser effect, the initially greater fighting capacity of males than females, and sex ratio. We expect its predictions to be general and suggest they be examined in a great number of species and taxa. Here, we test these predictions in four groups of wild vervet monkeys (Chlorocebus pygerythrus) in Mawana game reserve in Africa, using 7 years of data. We confirm that a higher proportion of males in the group is associated with greater dominance of females over males; a result that remains when combining these data with those of two other sites (Amboseli and Samara). We additionally confirm that in groups with a higher fraction of males there is a relatively higher (a) proportion of fights of males with other males, and (b) proportion of fights won by females against males from the fights of females with any adults. We reject alternative hypotheses that more dominance of females over males could be attributed to females receiving more coalitions from males, or females receiving lowered male aggression in exchange for sexual access (the docile male hypothesis). We conclude that female dominance relative to males is dynamic and that future empirical studies of inter-sexual dominance will benefit by considering the adult sex-ratio of groups.

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta).

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157-170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.

Complex sources of variance in female dominance rank in a nepotistic society.

Many mammalian societies are structured by dominance hierarchies, and an individual's position within this hierarchy can influence reproduction, behaviour, physiology and health. In nepotistic hierarchies, which are common in cercopithecine primates and also seen in spotted hyaenas, Crocuta crocuta, adult daughters are expected to rank immediately below their mother, and in reverse age order (a phenomenon known as 'youngest ascendancy'). This pattern is well described, but few studies have systematically examined the frequency or causes of departures from the expected pattern. Using a longitudinal data set from a natural population of yellow baboons, Papio cynocephalus, we measured the influence of maternal kin, paternal kin and group size on female rank positions at two life history milestones, menarche and first live birth. At menarche, most females (73%) ranked adjacent to their family members (i.e. the female held an ordinal rank in consecutive order with other members of her maternal family); however, only 33% of females showed youngest ascendancy within their matriline at menarche. By the time they experienced their first live birth, many females had improved their dominance rank: 78% ranked adjacent to their family members and 49% showed youngest ascendancy within their matriline. The presence of mothers and maternal sisters exerted a powerful influence on rank outcomes. However, the presence of fathers, brothers and paternal siblings did not produce a clear effect on female dominance rank in our analyses, perhaps because females in our data set co-resided with variable numbers and types of paternal and male relatives. Our results also raise the possibility that female body size or competitive ability may influence dominance rank, even in this classically nepotistic species. In total, our analyses reveal that the predictors of dominance rank in nepotistic rank systems are much more complex than previously thought.