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      Harem-holding males do not rise to the challenge: androgens respond to social but not to seasonal challenges in wild geladas

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          Abstract

          The challenge hypothesis has been enormously successful in predicting interspecific androgen profiles for vertebrate males. Nevertheless, in the absence of another theoretical framework, many researchers ‘retrofit’ the challenge hypothesis, so that its predictions also apply to intraspecific androgen comparisons. We use a wild primate, geladas ( Theropithecus gelada), to illustrate several considerations for androgen research surrounding male contests that do not necessarily fit within the challenge hypothesis framework. Gelada society comprises harem-holding males (that can mate with females) and bachelor males (that cannot mate with females until they take over a harem). Using 6 years of data from known males, we measured androgens (i.e. faecal testosterone (fT) metabolites) both seasonally and across specific male contests. Seasonal androgen variation exhibited a very different pattern than variation resulting from male contests. Although harem-holding males had higher testosterone levels than bachelors across the year, bachelors had higher testosterone during the annual ‘takeover season’. Thus, harem-holding males did not ‘rise to the challenge’ exactly when needed most. Yet, androgen profiles across male contests indicated that both sets of males exhibit the expected fT rise in response to challenges. Results from male geladas also support the idea that the context before (e.g. male condition) and after (e.g. contest outcome) a contest are critical variables for predicting hormones and behaviour.

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          Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes.

          Experience in aggressive contests often affects behaviour during, and the outcome of, later contests. This review discusses evidence for, variations in, and consequences of such effects. Generally, prior winning experiences increase, and prior losing experiences decrease, the probability of winning in later contests, reflecting modifications of expected fighting ability. We examine differences in the methodologies used to study experience effects, and the relative importance and persistence of winning and losing experiences within and across taxa. We review the voluminous, but somewhat disconnected, literature on the neuroendocrine mechanisms that mediate experience effects. Most studies focus on only one of a number of possible mechanisms without providing a comprehensive view of how these mechanisms are integrated into overt behaviour. More carefully controlled work on the mechanisms underlying experience effects is needed before firm conclusions can be drawn. Behavioural changes during contests that relate to prior experience fall into two general categories. Losing experiences decrease willingness to engage in a contest while winning experiences increase willingness to escalate a contest. As expected from the sequential assessment model of contest behaviour, experiences become less important to outcomes of contests that escalate to physical fighting.A limited number of studies indicate that integration of multiple experiences can influence current contest behaviour. Details of multiple experience integration for any species are virtually unknown. We propose a simple additive model for this integration of multiple experiences into an individual's expected fighting ability. The model accounts for different magnitudes of experience effects and the possible decline in experience effects over time. Predicting contest outcomes based on prior experiences requires an algorithm that translates experience differences into contest outcomes. We propose two general types of model, one based solely on individual differences in integrated multiple experiences and the other based on the probability contests reach the escalated phase. The difference models include four algorithms reflecting possible decision rules that convert the perceived fighting abilities of two rivals into their probabilities of winning. The second type of algorithm focuses on how experience influences the probability that a subsequent contest will escalate and the fact that escalated contests may not be influenced by prior experience. Neither type of algorithm has been systematically investigated.Finally, we review models for the formation of dominance hierarchies that assume that prior experience influences contest outcome. Numerous models have reached varied conclusions depending on which factors examined in this review are included. We know relatively little about the importance of and variation in experience effects in nature and how they influence the dynamics of aggressive interactions in social groups and random assemblages of individuals. Researchers should be very active in this area in the next decade. The role of experience must be integrated with other influences on contest outcome, such as prior residency, to arrive at a more complete picture of variations in contest outcomes. We expect that this integrated view will be important in understanding other types of interactions between individuals, such as mating and predator-prey interactions, that also are affected significantly by prior experiences.
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            Avoiding the ‘Costs’ of Testosterone: Ecological Bases of Hormone-Behavior Interactions

            A combination of laboratory and field investigations of birds has shown that expression of behavior such as territorial aggression can occur throughout the year in many species and in different life history stages. Although it is well known that testosterone regulates territorial aggression in males during the breeding season, the correlation of plasma testosterone and aggression appears to be limited to periods of social instability when a male is challenged for his territory by another male, or when mate-guarding a sexually receptive female. How essentially identical aggression is modulated in non-breeding life history stages is not fully resolved, but despite low circulating levels of testosterone outside the breeding season, expression of territorial aggression does appear to be dependent upon aromatization of testosterone and an estrogen receptor-mediated mechanism. There is accumulating evidence that prolonged high levels of circulating testosterone may incur costs that may potentially reduce lifetime fitness. These include interference with paternal care, exposure to predators, increased risk of injury, loss of fat stores and possibly impaired immune system function and oncogenic effects. We propose six hypotheses to explain how these costs of high testosterone levels in blood may be avoided. These hypotheses are testable and may reveal many mechanisms resulting from selection to avoid the costs of testosterone. It should also be noted that the hypotheses are applicable to vertebrates in general, and may also be relevant for other hormones that have a highly specialized suite of actions in one life history stage (such as breeding), but also have a limited action in other life history stages when the full spectrum of effects would be inappropriate.
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              The Steroid/Peptide Theory of Social Bonds: integrating testosterone and peptide responses for classifying social behavioral contexts.

              Hormones, and hormone responses to social contexts, are the proximate mechanisms of evolutionary pathways to pair bonds and other social bonds. Testosterone (T) is implicated in tradeoffs relevant to pair bonding, and oxytocin (OT) and arginine vasopressin (AVP) are positively tied to social bonding in a variety of species. Here, we present the Steroid/Peptide Theory of Social Bonds (S/P Theory), which integrates T and peptides to provide a model, set of predictions, and classification system for social behavioral contexts related to social bonds. The S/P Theory also resolves several paradoxes apparent in the literature on social bonds and hormones: the Offspring Defense Paradox, Aggression Paradox, and Intimacy Paradox. In the S/P Theory, we partition aggression into antagonistic and protective aggression, which both increase T but exert distinct effects on AVP and thus social bonds. Similarly, we partition intimacy into sexual and nurturant intimacy, both of which increase OT and facilitate social bonds, but exert distinct effects on T. We describe the utility of the S/P Theory for classifying 'tricky' behavioral contexts on the basis of their hormonal responses using partner cuddling, a behavior which is assumed to be nurturant but increases T, as a test case of the S/P Theory. The S/P Theory provides a comparative basis for conceptualizing and testing evolved hormonal pathways to pair bonds with attention to species, context, and gender/sex specificities and convergences. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society Publishing
                2054-5703
                September 2014
                24 September 2014
                24 September 2014
                : 1
                : 1
                : 140081
                Affiliations
                [1 ]Department of Anthropology, University of Michigan , Ann Arbor, MI 48109, USA
                [2 ]Department of Psychology, University of Michigan , Ann Arbor, MI 48109, USA
                Author notes
                Author for correspondence: David J. Pappano e-mail: dpappano@ 123456princeton.edu
                Author information
                http://orcid.org/0000-0003-3266-7531
                Article
                rsos140081
                10.1098/rsos.140081
                4448764
                faf8aed8-a085-4f1b-8b58-0ba21b521d3b
                © 2014 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 3 June 2014
                : 12 August 2014
                Categories
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                Custom metadata
                September, 2014

                challenge hypothesis,loser,male contest,seasonal,testosterone,winner

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