Female Marmosets' Behavioral and Hormonal Responses to Unfamiliar Intruders

Department of Cellular and Structural Biology, University of Texas Health Science Center, San Antonio, USA.
American Journal of Primatology (Impact Factor: 2.44). 10/2011; 73(10):1072-81. DOI: 10.1002/ajp.20975
Source: PubMed


The endocrine control mechanisms for female mammalian aggression have been largely unstudied. Although it has been proposed that androgens may modulate female aggressive behavior in a similar manner to males, very little conclusive evidence exists. Previous work in male marmosets found that post-encounter increases in testosterone (T) were dependent on the intensity of aggression displayed during the aggressive encounter. We exposed female marmosets (Callithrix kuhlii), a monogamous and biparental primate, to aggressive interactions with unfamiliar intruders. Individual female marmosets exhibited changes in T and estradiol (E(2) ) that are associated with aggressiveness dependent on the intensity of aggression displayed as well as their role during the encounter. Resident females exhibited increased E(2) immediately following an encounter in which they displayed high rates of aggression. If resident females received high rates of aggression from the intruder, the resident displayed increased T 24 hr following the encounter. Interestingly, if the female was an intruder in the encounter, the intensity of her aggression was associated with increased cortisol immediately following the trials, whereas received aggression was associated with increased T and E(2) immediately following the trial. Female primates do exhibit situation-dependent changes in gonadal steroids in association with aggression that may serve to prime them for future aggressive interactions.

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    • "These tests have typically been carried out with live stimulus animals, either viewed through a grate or down a long chute in a testing apparatus. Similar live intruder tests have been carried out in other New World monkey species to examine sex differences in reactions to strangers [Wolovich et al., 2010], hormonal responses to intruders [Ross & French, 2011], and effects of group size [Schaffner & French, 1997] among other variables. For New World monkeys, such as the titi monkey, a mirror image is likely viewed as a samesex stranger [Anderson & Gallup, 2011b]. "
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    ABSTRACT: Mate-guarding and territorial aggression (both intra- and inter-sexual) are behavioral components of social monogamy seen in male coppery titi monkeys (Callicebus cupreus) both in the field and in the laboratory. Methodology for studying these behaviors in captivity facilitates the translation of questions between field and laboratory. In this study, we tested whether exposure to a mirror would stimulate mate-guarding behavior in male titi monkeys, and whether this exposure was accompanied by hormonal changes. Eight males were exposed to a mirror condition (treatment) or the back of the mirror (control) for five sessions, and behavioral responses were filmed. Blood samples were taken to measure levels of cortisol, oxytocin, and vasopressin. Lipsmacks (P < 0.0001), arching (P < 0.0001), tail-lashing (P = 0.009), restraining (P = 0.015), and approaches to the female (P = 0.0002) were all higher during the mirror condition, while tail-twining tended to decline during the mirror condition (P = 0.076). Hormones did not vary by experimental treatment, but were correlated with certain behaviors during the presentation of the mirror. While social behaviors changed with mirror exposure, self-directed and mirror-guided behaviors did not, indicating a lack of self-recognition. Use of a mirror was a safe and effective means of investigating mate-guarding behavior in response to a simulated intrusion, with the added benefit of not needing another animal to serve as an intruder; and thus may be of use in providing a laboratory model for natural behavior. Especially, as it eliminates the need for a stimulus animal, it would also be of possible use in investigating responses to a simulated intruder in wild populations of titis and other pithecines. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.
    American Journal of Primatology 09/2015; DOI:10.1002/ajp.22483 · 2.44 Impact Factor
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    • "Cooperatively-breeding callitrichine primates also exhibit higher social tolerance for, and opportunistic behavioral strategies with, opposite-sex strangers, especially in the absence of their pairmate. For instance, both adult male and female wild marmosets engage in extra-group sociosexual behavior during the course of intergroup encounters (Digby, 1999; Lazaro-Perea, 2001; Nievergelt et al., 2000); and socially-bonded adult tamarins and marmosets participate in high rates of opportunistic social and sexual interactions with opposite-sex strangers when the established partner is absent, and social indifference or aggression toward the oppositesex stranger when the partner is present (Inglett et al., 1990; Ross and French, 2011). In this fashion, the nature of social monogamy in callitrichine primates may more closely resemble the opportunistic strategies associated with partner fidelity in both female (Gangestad et al., 2010) and male (Buss, 2013) humans, and less like the nature of pair relationships in prairie voles, which are characterized by high social selectivity for partners (Rodriguez et al., 2013). "
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    ABSTRACT: Cooperatively-breeding and socially-monogamous primates, like marmosets and humans, exhibit high levels of social tolerance and prosociality toward others. Oxytocin (OXT) generally facilitates prosocial behavior, but there is growing recognition that OXT modulation of prosocial behavior is shaped by the context of social interactions and by other motivational states such as arousal or anxiety. To determine whether prosociality varies based on social context, we evaluated whether marmoset donors (Callithrix penicillata) preferentially rewarded pairmates versus opposite-sex strangers in a prosocial food-sharing task. To examine potential links among OXT, stress systems, and prosociality, we evaluated whether pretrial cortisol levels in marmosets altered the impact of OXT on prosocial responses. Marmosets exhibited spontaneous prosociality toward others, but they did so preferentially toward strangers compared to their pairmates. When donor marmosets were treated with marmoset-specific Pro(8)-OXT, they exhibited reduced prosociality toward strangers compared to marmosets treated with saline or consensus-mammalian Leu(8)-OXT. When pretrial cortisol levels were lower, marmosets exhibited higher prosociality toward strangers. These findings demonstrate that while marmosets show spontaneous prosocial responses toward others, they do so preferentially toward opposite-sex strangers. Cooperative breeding may be associated with the expression of prosociality, but the existence of a pair-bond between marmoset partners appears to be neither necessary nor sufficient for the expression of spontaneous prosocial responses. Further, high prosociality toward strangers is significantly reduced in marmosets treated with Pro(8)-OXT, suggesting that OXT does not universally enhance prosociality, but, rather OXT modulation of prosocial behavior varies depending on social context. Copyright © 2015. Published by Elsevier Inc.
    Hormones and Behavior 05/2015; 71:83-90. DOI:10.1016/j.yhbeh.2015.04.015 · 4.63 Impact Factor
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    ABSTRACT: Female-female aggression often functions in competition over reproductive or social benefits, but the proximate mechanisms of this apparently adaptive behaviour are not well understood. The sex steroid hormone testosterone (T) and its metabolites are well-established mediators of male-male aggression, and several lines of evidence suggest that T-mediated mechanisms may apply to females as well. However, a key question is whether mechanisms of female aggression primarily reflect correlated evolutionary responses to selection acting on males, or whether direct selection acting on females has made modifications to these mechanisms that are adaptive in light of female life history. Here, I examine the degree to which female aggression is mediated at the level of T production, target tissue sensitivity to T, or downstream genomic responses in order to test the hypothesis that selection favours mechanisms that facilitate female aggression while minimizing the costs of systemically elevated T. I draw heavily from avian systems, including the dark-eyed junco (Junco hyemalis), as well as other organisms in which these mechanisms have been well studied from an evolutionary/ecological perspective in both sexes. Findings reveal that the sexes share many behavioural and hormonal mechanisms, though several patterns also suggest sex-specific adaptation. I argue that greater attention to multiple levels of analysis-from hormone to receptor to gene network, including analyses of individual variation that represents the raw material of evolutionary change-will be a fruitful path for understanding mechanisms of behavioural regulation and intersexual coevolution.
    Philosophical Transactions of The Royal Society B Biological Sciences 01/2013; 368(1631):20130083. DOI:10.1098/rstb.2013.0083 · 7.06 Impact Factor
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