Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

Hormonal correlates of social status and courtship display in the cooperatively lekking lance-tailed manakin

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations.     

Raising Darwin’s consciousness

Sociobiologists and feminists agree that men in patriarchal social systems seek to control females, but sociobiologists go further, using Darwin’s theory of sexual selection and Trivers’s ideas on parental investment to explain why males should attempt to control female sexuality. From this perspective, the stage for the development under some conditions of patriarchal social systems was set over the course of primate evolution. Sexual selection encompasses both competition between males and female choice. But in applying this theory to our “lower origins” (prehominid ancestors), Darwin assumed that choices were made by essentially “coy” females. I argue here that female solicitation of multiple males (either simultaneously or sequentially, depending on the breeding system) characterized prehominid females; this prehominid legacy of cyclical sexual assertiveness, itself possibly a female counter-strategy to male efforts to control the timing of female reproduction, generated further male counter-strategies. This dialectic had important implications for emerging hominid mating systems, human evolution, and the development of patriarchal arrangements in some human societies. For hominid males who will invest in offspring, there would be powerful selection for emotions, behaviors, and customs that ensure them certainty of paternity. The sexual modesty that so struck Darwin can be explained as a recent evolved or learned (perhaps both) adaptation in women to avoid penalties imposed by patrilines on daughters and mates who failed to conform to the patriline’s prevailing norms for their sex. Other supposedly innate universals, such as female preferences for wealthy husbands, are also likely to be facultative accommodations by women to constraints set up when patrilines monopolized resources needed by females to survive and reproduce, and passed on intergenerational control of these resources preferentially to sons.     

It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird

Variance in reproductive success among individuals is a defining characteristic of many social vertebrates. Yet, our understanding of which male attributes contribute to reproductive success is still fragmentary in most cases. Male–male reproductive coalitions, where males jointly display to attract females, are of particular interest to evolutionary biologists because one male appears to forego reproduction to assist the social partner. By examining the relationship between social behaviour and reproductive success, we can elucidate the proximate function of coalitions in the context of mate choice. Here, we use data from a 4-year study of wire-tailed manakins (Pipra filicauda) to provide molecular estimates of reproductive skew and to test the hypothesis that male–male social interactions, in the context of coordinated displays, positively influence a male''s reproductive success. More specifically, we quantify male–male social interactions using network metrics and predict that greater connectivity will result in higher relative reproductive success. Our data show that four out of six leks studied had significant reproductive skew, with success apportioned to very few individuals in each lek. Metrics of male social affiliations derived from our network analysis, especially male connectivity, measured as the number of males with whom the focal male has extended interactions, were strong predictors of the number of offspring sired. Thus, network connectivity is associated with male fitness in wire-tailed manakins. This pattern may be the result of shared cues used by both sexes to assess male quality, or the result of strict female choice for coordinated display behaviour.     

Social behaviors within a group of captive female Hippopotamus amphibius

Grouping is known to occur in many species of mammals, and the structure of groups can range along a continuum from basic aggregations to complex social systems. Any social patterns that may occur within the group must be determined in order to understand the adaptive nature of the group. Female Hippopotamus amphibius are known to aggregate in the wild, but their social behaviors are still not understood. Our objective was to determine if captive female hippos display social structure within an aggregation by examining their interactions, and if kinship, familiarity, and dominance influence these interactions. Behavioral data, using continuous focal animal sampling and scan sampling, were collected on a group of captive female hippos housed at Disney’s Animal Kingdom and were used to analyze their interactions, association patterns based on kinship and familiarity, and a dominance hierarchy. Our results support the hypothesis that hippos exhibit social patterns due to the attraction to particular individuals. There were more associations between kin than non-kin and also between individuals that were more familiar. Dominance patterns were also found among these hippos. These results may aid in the general understanding of hippopotamus behavior and provide a framework for future research.     

Mate Choice Copying in Humans

There is substantial evidence that in human mate choice, females directly select males based on male display of both physical and behavioral traits. In non-humans, there is additionally a growing literature on indirect mate choice, such as choice through observing and subsequently copying the mating preferences of conspecifics (mate choice copying). Given that humans are a social species with a high degree of sharing information, long-term pair bonds, and high parental care, it is likely that human females could avoid substantial costs associated with directly searching for information about potential males by mate choice copying. The present study was a test of whether women perceived men to be more attractive when men were presented with a female date or consort than when they were presented alone, and whether the physical attractiveness of the female consort affected women’s copying decisions. The results suggested that women’s mate choice decision rule is to copy only if a man’s female consort is physically attractive. Further analyses implied that copying may be a conditional female mating tactic aimed at solving the problem of informational constraints on assessing male suitability for long-term sexual relationships, and that lack of mate choice experience, measured as reported lifetime number of sex partners, is also an important determinant of copying.     

Behavioral solutions to breeding cheetahs in captivity: Insights from the wild

Knowledge of cheetahs' behavior is increasingly seen as the key to solving the mystery of cheetahs' poor breeding performance in captivity. In the absence of zoos' maintaining systematic records of individuals' behavior during introductions, behavior of free-living animals can be informative. In the wild, most female cheetahs probably mate with males living in small groups or coalitions; thus, zoos may benefit from replicating these social conditions, provided injuries can be minimized. Relations between free-living coalition members are amicable, and escalated aggression was never witnessed during 4 years of observation. Some antagonism was seen in newly formed trios, although this had disappeared in longer established coalitions. Minor aggression occurred over carcasses, being greater at small and intermediate sized kills than at large ones. In the presence of females, mild intramale aggression was only seen within 1 of 7 coalitions. Free-living females showed similar rates of behavior in the presence of different numbers of males, aside from more frequent growling at large groups. These findings suggest that captive institutions should be less nervous about housing male cheetahs together and introducing females to groups of males for purposes of breeding. © 1993 Wiley-Liss, Inc.     

Construction of cell surface-engineered yeasts displaying antigen to detect antibodies by immunofluorescence and yeast-ELISA

In order to detect monoclonal antibodies (MAbs) from insufficient and unavailable human proteins, yeast cells were engineered to display human antigens on their surface and consequently endowed with the ability to specifically bind antibodies. Thus, a fusion gene for the expression of the human proteasome subunit alpha 6 (hPSA6) and human profilin I (hProI) were assembled, respectively, with a His.tag marker at the C-terminal and displayed on yeast surface. With anti-His.tag MAb as the primary antibody and the fluorescein isothiocyanate-conjugated goat anti-mouse Immunoglobulin G as the second antibody, the surface display of hPSA6 and hProI were verified by immunofluorescence labeling. The antigen-displayed yeast particles were used for MAbs detection from ascites through both immunofluorescence and yeast-enzyme-linked immunosorbent assay (ELISA) methods. The results were verified by Western blotting and indirect ELISA. By improving the sensitivity, the novel MAbs detection can be applied in the generation and screening of positive hybridoma. It is suggested that by combining the DNA immunization, the present study can evolve into a quick and protein-free way of MAbs production for insufficient and unavailable antigen.     

Mate choice in modern societies

Most research on mate choice in modern societies is based on data that may or may not reflect actual mating behavior (e.g., stated preferences, personal advertisements). In the present study, real-life matings were reported by a large representative sample of men and women (N = 1,133). These data were used to test an evolutionary model in which mate choice is hypothesized to depend on resources potentially contributed to reproduction by each sex. Consistent with the model, it was found that (a) men (but not women) of higher social status acquire more mating partners, suggesting that male status is an important criterion in female choice; (b) women’s (but not men’s) number of partners decreases linearly with age, suggesting that female reproductive potential is an important criterion in male choice; and (c) women (but not men) display a significant relationship between marital dissolution and promiscuity, suggesting that female sexual exclusivity is an important criterion in male choice. These results are discussed in relation to understanding mate choice mechanisms from behavioral data. Daniel Pérusse is an assistant professor in the Department of Anthropology at the Université de Montréal. His research interests include the evolutionary biology of human social and reproductive behavior, sexual selection theory, and biocultural evolution. His current research bears on human socialization processes and psychosocial development from an evolutionary and behavior-genetic perspective. Recent publications include “Cultural and Reproductive Success in Industrial Societies: Testing the Relationship at the Proximate and Ultimate Levels” (Behavioral and Brain Sciences 16(2):267–322, 1993) and “Human Parental Behavior: Evidence for Genetic Influence and Potential Implications for Gene-Culture Theory” with M. C. Neale, A. Heath, and L. J. Eaves (Behavior Genetics, in press).     

小型田鼠:研究单配制进化与调控的模型

哺乳动物的单配制通常被认为是社会性单配制,它不是单纯地由性行为来决定,而是由诸多因素,包括长期的pair bond、夫妻双方共同抚育后代、免近亲交配以及雌雄两性相似等来决定的。在这篇综述中,我们论述了如何以啮齿类田鼠属(Microtus)为模型,通过比较研究来帮助我们理解社会性单配制的进化以及其神经调控机制。对田鼠属的研究不仅证实了单配制起源于艰苦的生存条件的假说,而且还证实了雌性性选择可能有利于维持单配制。不仅如此,哺乳动物单配制的进化还需要雄性的prosocial行为的不断强化。例如,亲近行为可以促进pairbond的形成并强化雄性对后代的哺育行为,而这种强化则来源于神经多肽催产素(OT)和加压素(AVP)与类固醇类激素的相互作用。催产素和加压素调控pairbond和双亲哺育行为的表达,而单配制和多配制田鼠的催产素和加压素受体在脑内的分布有显的不同。比较研究揭示了小型田鼠单配制的调控机制,而种内差异和行为上的可塑性则有助于我们进一步理解这种机制。比如,在某些条件下,多配制的草原田鼠(Microtus pennsylvanicu)的雄性个体具有哺育后代的行为。尽管草原田鼠的加压素Vla受体在脑内的分布与其他多配制的田鼠相似,但是如果脑室注射加压素,仍可以诱发其哺育后代的行为。同样是单配制的橙腹田鼠(Microtus ochrogaster),生活在：Illnois的显示出高水平的prosocial行为,而生活在Kansas的则表现出较低水平的社会性行为。即使两个种群的催产素或加压素Vla受体在脑内的分布相同,它们的雌激素受体表达水平显不同,这在雄性个体表现尤其明显。与Kansas的雄性个体相比,在终纹床核(bed rucleus of the stria tenninalis)和杏仁核中区(medial amygdala)这两个调控亲近行为和攻击行为的脑区,Illinois的雄性个体的α雌激素受体的水平要低得多。这些研究表明对雌激素的低敏感程度有利于高水平地表达prosocial行为并降低特定类型的攻击行为。     

Dynamics of alliance formation and the egalitarian revolution

Background

Arguably the most influential force in human history is the formation of social coalitions and alliances (i.e., long-lasting coalitions) and their impact on individual power. Understanding the dynamics of alliance formation and its consequences for biological, social, and cultural evolution is a formidable theoretical challenge. In most great ape species, coalitions occur at individual and group levels and among both kin and non-kin. Nonetheless, ape societies remain essentially hierarchical, and coalitions rarely weaken social inequality. In contrast, human hunter-gatherers show a remarkable tendency to egalitarianism, and human coalitions and alliances occur not only among individuals and groups, but also among groups of groups. These observations suggest that the evolutionary dynamics of human coalitions can only be understood in the context of social networks and cognitive evolution.

Methodology/Principal Findings

Here, we develop a stochastic model describing the emergence of networks of allies resulting from within-group competition for status or mates between individuals utilizing dyadic information. The model shows that alliances often emerge in a phase transition-like fashion if the group size, awareness, aggressiveness, and persuasiveness of individuals are large and the decay rate of individual affinities is small. With cultural inheritance of social networks, a single leveling alliance including all group members can emerge in several generations.

Conclusions/Significance

We propose a simple and flexible theoretical approach for studying the dynamics of alliance emergence applicable where game-theoretic methods are not practical. Our approach is both scalable and expandable. It is scalable in that it can be generalized to larger groups, or groups of groups. It is expandable in that it allows for inclusion of additional factors such as behavioral, genetic, social, and cultural features. Our results suggest that a rapid transition from a hierarchical society of great apes to an egalitarian society of hunter-gatherers (often referred to as “egalitarian revolution”) could indeed follow an increase in human cognitive abilities. The establishment of stable group-wide egalitarian alliances creates conditions promoting the origin of cultural norms favoring the group interests over those of individuals.     

On the Perception of Newcomers

Human coalitions frequently persist through multiple, overlapping membership generations, requiring new members to cooperate and coordinate with veteran members. Does the mind contain psychological adaptations for interacting within these intergenerational coalitions? In this paper, we examine whether the mind spontaneously treats newcomers as a motivationally privileged category. Newcomers—though capable of benefiting coalitions—may also impose considerable costs (e.g., they may free ride on other members, they may be poor at completing group tasks). In three experiments we show (1) that the mind categorizes coalition members by tenure, including newcomers; (2) that tenure categorization persists in the presence of orthogonal and salient social dimensions; and (3) that newcomers elicit a pattern of impressions consistent with their probable ancestral costs. These results provide preliminary evidence for a specialized component of human coalitional psychology: an evolved concept of newcomer.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Estrogen mitogenic action. II. Negative regulation of the steroid hormone-responsive growth of cell lines derived from human and rodent target tissue tumors and conceptual implications

Summary In an accompanying report (Moreno-Cuevas, J. E.; Sirbasku, D. A., In Vitro Cell. Dev. Biol.; 2000), we demonstrated 80-fold estrogen mitogenic effects with MTW9/PL2 rat mammary tumor cells in cultures supplemented with charcoaldextran-treated serum. All sera tested contained an estrogen reversible inhibitor(s). The purpose of this report is to extend those observations to additional sex steroid-responsive human and rodent cell lines. Every line tested showed a biphasic response to hormone-depleted serum. Concentrations of ≤10% (v/v) promoted substantive growth. At higher concentrations, serum was progressively inhibitory. With estrogen receptor-positive (ER⁺) human breast cancer cells, rat pituitary tumor cells, and Syrian hamster kidney tumor cells, 50% (v/v) serum caused significant inhibition, which was reversed by very low physiologic concentrations of estrogens. This same pattern was observed with the steroid hormone-responsive LNCaP human prostatic carcinoma cells. Because steroid hormone mitogenic effects are now easily demonstrable using our new methods, the identification of positive results has nullified our original endocrine estromedin hypothesis. We also evaluated autocrine/paracrine growth factor models of estrogen-responsive growth. We asked if insulin-like growth factors I and II, insulin, transforming growth factor alpha, or epidermal growth factor substituted for the positive effects of estrogens. Growth factors did not reverse the serum-caused inhibition. We asked also if transforming growth factor beta (TGFβ) substituted for the serum-borne inhibitor. TGFβ did not substitute. Altogether, our results are most consistent with the concept of a unique serum-borne inhibitor as has been proposed in the estrocolyone model. However, the aspect of the estrocolyone model related to steroid hormone mechanism of action requires more evaluation. The effects of sex steroids at picomolar concentrations may reflect mediation via inhibitor “activated” intracellular signaling pathways.     

Cultural variation is part of human nature

In 1966, Laura Bohannan wrote her classic essay challenging the supposition that great literary works speak to universal human concerns and conditions and, by extension, that human nature is the same everywhere. Her evidence: the Tiv of West Africa interpret Hamlet differently from Westerners. While Bohannan’s essay implies that cognitive universality and cultural variation are mutually exclusive phenomena, adaptationist theory suggests otherwise. Adaptive problems ("the human condition") and cognitive adaptations ("human nature") are constant across cultures. What differs between cultures is habitat: owing to environmental variation, the means and information relevant to solving adaptive problems differ from place to place. Thus, we find differences between cultures not because human minds differ in design but largely because human habitats differ in resources and history. On this view, we would expect world literature to express both human universals and cultural particularities. Specifically, we should expect to find literary universality at the macro level (e.g., adaptive problems, cognitive adaptations) and literary variation at the micro level (e.g., local solutions to adaptive problems).     

Factors affecting life and death in Serengeti cheetahs: environment, age, and sociality

We examined environmental and social factors affecting reproductivesuccess across a 20-year data set of individually known cheetahson the Serengeti Plains of Tanzania. Because cheetahs are seeninfrequently and are not amenable to mark–recapture techniques,we devised a model to estimate time of death for individualsthat disappeared from our records. We found that males had markedlylower survival than females. Recruitment was negatively affectedby rainfall but positively affected by numbers of Thomson'sgazelles, the cheetahs' chief prey. There was a negative associationbetween recruitment and numbers of lions, demonstrating thatthe high rates of predation observed in previous studies haveimplications for the dynamics of cheetah populations. Recruitmentwas related to mother's age, peaking when she reached 6–7years. Sociality affected survival in two ways. First, adolescentsliving in temporary sibling groups had higher survival thansingletons, particularly males with sisters. Second, adult malesliving in coalitions had higher survival than singletons inperiods when other coalitions were numerous, yet they had lowersurvival when other coalitions were rare. These results corroborateobservations of enhanced prey capture by female adolescentsand antipredator benefits for adolescents in groups, as wellas competitive advantages for adult males in groups. Furthermore,our findings stress the importance of interactions between environmentaland social factors in affecting reproductive success in mammals.     

The similarity principle underlying social bonding among female rhesus monkeys

Twenty adult female rhesus monkeys (Macaca mulatta) were observed over a three-year period. They lived in a mixed captive group with kinship relations known for three generations. The study's aim was to test Seyfarth's [J. theor. Biol. 65: 671-698, 1977] model of rank-related grooming and to investigate two other possible determinants of social bonding, i.e. relative age and the group's stratification into two social classes. Data on affiliation, coalitions, and social competition were collected by means of both focal observation and instantaneous time sampling. Whereas certain elements of the existing model were confirmed, its explanatory principles were not. Social competition did not result in more contact among close-ranking females (the opposite effect was found), and the relation between affiliative behavior and coalitions was more complex than predicted. Based on multivariate analyses and a comparison of theoretical models, we propose a simpler, more encompassing principle underlying interfemale attraction. According to this 'similarity principle', rhesus females establish bonds with females whom they most resemble. The similarity may concern genetical and social background, age, hierarchical position and social class. Effects of these four factors were independently demonstrated. The most successful model assumed that similarity factors influence female bonding in a cumulative fashion.     

Food calling by captive bonobos (Pan paniscus): An experiment

We examined (i) whether bonobos display a specific food-calling behavior when discovering a hidden food resource, (ii) whether the presence of competitors affects this behavior, and (iii) whether food quantity or gender influences its appearance. We carried out experiments (n = 108) within a captive group of eight bonobos at the Animal Park Planckendael (Mechelen,Belgium). We hid highly preferred food items (n = 7 or 25) in their enclosure and recorded vocal behavior and interactions between discoverer and group members. As a control, we gave the same number of items to the individuals when isolated from the group, a situation without potential food competition (n = 38). The only vocalization frequently uttered by the discoverer was the food peep. They uttered food peeps significantly more often when no food competition was possible. The amount of food had no significant influence on whether food peeps were uttered. The same applies to the individuals’ identity or gender. Although the costs of food calling behavior seemed much higher for males, both sexes uttered food calls to the same extent. We hypothesize thai males signal food presence in order to attract potential mates and are willing to give up the discovered food resource in return for sex: sex for food exchange. In contrast, females may vocalize to attract coalition partners. Through these coalitions, they can monopolize food resources vis-à-vis males. It is also possible that females have less reason to suppress food calk, since they are dominant to males. This study suggests that bonobos are able to give shaded signals about their environment and have the potential to communicate this information in order to promote their sexual strategy.     

Dispersal in Kin Coalition Throughout the Non‐Breeding Season to Facilitate Fine‐Scale Genetic Structure in the Breeding Season: Evidence From a Small Passerine

Evidence shows that social cooperation among kin may evolve even in birds with extensive dispersal. In such cases, maintaining kinship during dispersal is essential to the subsequent expression of kin cooperation. This hypothesis has not been examined for most bird species. We addressed it in the ground tit (Parus humilis), a passerine where kin frequently interact in terms of cooperative polygamy and extra‐pair mating despite fast annual turnover of the breeding population. Pedigree and genotype data showed that while groups varied in composition throughout the non‐breeding season due to continual individual emigration and immigration, they always contained kin coalitions consisting of either local or immigrant individuals of different age and sexes. The first‐order kin coalitions, according to the information from local individuals, stemmed from single‐family lineages (siblings and their parents), and the lower‐order ones from neighbouring, related family lineages that merged after fledging. It was probable that immigrants had formed kin coalitions in similar ways before dispersing. Groups broke up in the breeding season. Pairing between unrelated individuals from different coalitions within a group was more likely, whereas related individuals from the same coalition tended to nest near each other. The resulting fine‐scale population genetic structure is expected to facilitate breeding interactions among kin. Our findings give clues to understanding the evolution of social cooperation in relation to dispersal.