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John C Wingfield - One of the best experts on this subject based on the ideXlab platform.
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Testosterone, Territoriality, and Social Interactions in Neotropical Birds
Sexual Selection, 2020Co-Authors: John C Wingfield, Rodrigo A. Vásquez, Ignacio T MooreAbstract:Abstract Our understanding of hormone–behavior relationships is largely based on studies of northern latitude species. Such studies have greatly expanded our general knowledge of the role of testosterone in free-living animals, particularly birds. Results from such studies have resulted in the development of the Challenge Hypothesis, which posits that testosterone levels rise above those necessary for reproduction due to social interactions. However, the vast majority of animals inhabit the tropics and have very different life histories as a consequence. In fact, many southern latitude species have life histories more like tropical species than like their counterparts from northern latitudes. The broad applicability of the findings based on northern species is thus questionable. Based on the few studies of neotropical birds, it appears testosterone and its role in reproduction and social interactions are very different from northern species. Testosterone levels do not elevate in response to male–male interactions, and blocking testosterone does not suppress territorial intrusions. Further studies of both tropical and southern latitude species are thus warranted to develop a broader and deeper understanding of testosterone and its role in reproduction and associated territorial aggression.
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whither the Challenge Hypothesis
Hormones and Behavior, 2020Co-Authors: John C Wingfield, Marilyn Ramenofsky, Robert E Hegner, Gregory F BallAbstract:Abstract Almost fifty years ago the advent of assay methods to measure circulating levels of hormones revolutionized endocrinology in relation to investigations of free-living and captive animals. This new field “environmental endocrinology” revealed that endocrine profiles in animals in their natural habitat were not only different from captive animals, but often deviated from predictions. It quickly became apparent that the organization and analysis of data from the field should be sorted by life history stages such as for reproductive processes, migration, molt etc. and spaced in time according to natural duration of those processes. Presentation of data by calendar date alone gives much simpler, even misleading, patterns. Stage-organized analyses revealed species-specific patterns of hormone secretion and dramatic inter-individual differences. The “Challenge Hypothesis” sparked exploration of these results, which diverged from expectations of hormone-behavior interactions. The Hypothesis led to specific predictions about how the hypothalamo-pituitary-gonad axis, and particularly circulating patterns of testosterone, might respond to social Challenges such as simulated territorial intrusions. Initially, a group of studies on free-living and captive birds played a key role in the formulation of the Hypothesis. Over the decades since, the effects of social Challenge and environmental context on hormonal responses have been tested in all vertebrate taxa, including humans, as well as in insects. Although it is now clear that the Challenge Hypothesis in its original form is simplistic, field and laboratory tests of the Hypothesis have led to other concepts that have become seminal to the development of environmental endocrinology as a field. In this special issue these developments are addressed and examples from many different taxa enrich the emerging concepts, paving the way for investigations using recent technologies for genetic and transcriptome analyses.
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reprint of concepts derived from the Challenge Hypothesis
Hormones and Behavior, 2020Co-Authors: John C Wingfield, Wolfgang Goymann, Cecilia Jalabert, Kiran K SomaAbstract:Abstract The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The Hypothesis has been tested many times over the past 30 years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the Hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social Challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.
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concepts derived from the Challenge Hypothesis
Hormones and Behavior, 2019Co-Authors: John C Wingfield, Wolfgang Goymann, Cecilia Jalabert, Kiran K SomaAbstract:Abstract The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The Hypothesis has been tested many times over the past 30 years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the Hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social Challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.
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the Challenge Hypothesis where it began and relevance to humans
Hormones and Behavior, 2017Co-Authors: John C WingfieldAbstract:Abstract A contribution to a special issue on Hormones and Human Competition. Over 40 years ago assay methods that allowed the accurate measurement of circulating levels of hormones were developed for the first time enabling us to sample free-living as well as captive animals. This led to a new concept called “field endocrinology”. It quickly became apparent that endocrine profiles of animals under natural conditions were very different from congeners in captivity. Furthermore, hormone data could be organized by functional units (e.g. reproductive states) spaced in time according to natural duration of those states rather than simply by date alone. This approach changed how we interpret data and revealed species-specific patterns of hormone secretion. The “Challenge Hypothesis”, stating that the temporal patterns of testosterone in blood were determined by a trade-off between the degree of male-male competition that increased testosterone, and the expression of paternal care that required a decrease in testosterone, grew out of a combination of field endocrine investigations that then informed laboratory experimentation. A strong argument can now be made that the Challenge Hypothesis is highly relevant for understanding social interactions in humans and non-human primates. Investigations on human subjects provide some of the best models for the Challenge Hypothesis. However, the central mechanisms by which aggressive and other social interactions regulate the hypothalamo-pituitary-gonad axis will depend upon work on not only primates, but also other vertebrates in very different ecological contexts. Research on the Challenge Hypothesis in humans will play a critical role as new insight on the interrelationships of testosterone and male-male competition comes from new technologies.
Wolfgang Goymann - One of the best experts on this subject based on the ideXlab platform.
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reprint of concepts derived from the Challenge Hypothesis
Hormones and Behavior, 2020Co-Authors: John C Wingfield, Wolfgang Goymann, Cecilia Jalabert, Kiran K SomaAbstract:Abstract The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The Hypothesis has been tested many times over the past 30 years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the Hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social Challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.
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who rises to the Challenge testing the Challenge Hypothesis in fish amphibians reptiles and mammals
Hormones and Behavior, 2020Co-Authors: Ignacio T Moore, Jessica Hernandez, Wolfgang GoymannAbstract:Abstract According to the Challenge Hypothesis, social interactions, particularly among males, have a strong influence on circulating androgen levels. Specifically, males should respond to social Challenges from conspecific males with a rapid increase in plasma androgen levels which support and stimulate further aggression. This basic tenet of the Challenge Hypothesis, an androgen increase in response to a social Challenge from another male, has been tested in all vertebrate classes. While early studies generally supported the Challenge Hypothesis, more recent work has noted numerous exceptions, particularly in birds. Here, we conduct a meta-analysis of studies in fish, amphibians, non-avian reptiles, and mammals that test the prediction that circulating androgen levels of males should increase in response to an experimental Challenge from another male. We found that teleost fish often increase androgens during such Challenges, but other vertebrate groups show more mixed results. Why should fish be different from the other taxa? In fish with paternal care of young, the potential conflict between mating, being aggressive towards other males, and taking care of offspring is alleviated, because females typically choose males based on their defense of an already existing nest. Hence, rather than regulating the trade-off between mating, aggression, and parenting, androgens may have been co-opted to promote all three behaviors. For other taxa, increasing androgen levels only makes sense when the increase directly enhances reproductive success. Thus, the increase in androgen levels is a response to mating opportunities rather than a response to Challenge from another male. To further our understanding of the role of a change in androgen levels in mediating behavioral decision-making between mating, aggression, and parenting, we need studies that address the behavioral consequences of an increase in androgens after male-male encounters and studies that test the androgen responsiveness of species that differ in the degree of paternal care.
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concepts derived from the Challenge Hypothesis
Hormones and Behavior, 2019Co-Authors: John C Wingfield, Wolfgang Goymann, Cecilia Jalabert, Kiran K SomaAbstract:Abstract The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The Hypothesis has been tested many times over the past 30 years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the Hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social Challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.
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Experimental induction of social instability during early breeding does not alter testosterone levels in male black redstarts, a socially monogamous songbird.
Hormones and Behavior, 2013Co-Authors: Camila Patricia Villavicencio, Beate A. Apfelbeck, Wolfgang GoymannAbstract:Testosterone plays an important role in territorial behavior of many male vertebrates and the Challenge Hypothesis has been suggested to explain differences in testosterone concentrations between males. For socially monogamous birds, the Challenge Hypothesis predicts that testosterone should increase during male–male interactions. To test this, simulated territorial intrusion (STI) experiments have been conducted, but only about a third of all bird species investigated so far show the expected increase in testosterone. Previous studies have shown that male black redstarts (Phoenicurus ochruros) do not increase testosterone during STIs or short-term male–male Challenges. The aim of this study was to evaluate whether black redstarts modulate testosterone in an experimentally induced longer-term unstable social situation. We created social instability by removing males from their territories and compared the behavior and testosterone concentrations of replacement males and neighbors with those of control areas. Testosterone levels did not differ among replacement males, neighbors and control males. Injections with GnRH resulted in elevation of testosterone in all groups, suggesting that all males were capable of increasing testosterone. We found no difference in the behavioral response to STIs between control and replacement males. Furthermore, there was no difference in testosterone levels between replacement males that had expanded their territory and new-coming males. In combination with prior work these data suggest that testosterone is not modulated by male–male interactions in black redstarts and that testosterone plays only a minor role in territorial behavior. We suggest that territorial behavior in species that are territorial throughout most of their annual life-cycle may be decoupled from testosterone.
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Ignoring the Challenge? Male black redstarts (Phoenicurus ochruros) do not increase testosterone levels during territorial conflicts but they do so in response to gonadotropin-releasing hormone.
Proceedings of The Royal Society B: Biological Sciences, 2011Co-Authors: Beate A. Apfelbeck, Wolfgang GoymannAbstract:Competition elevates plasma testosterone in a wide variety of vertebrates, including humans. The ‘Challenge Hypothesis’ proposes that seasonal peaks in testosterone during breeding are caused by social Challenges from other males. However, during experimentally induced male–male conflicts, testosterone increases only in a minority of songbird species tested so far. Why is this so? Comparative evidence suggests that species with a short breeding season may not elevate testosterone levels during territory defence. These species may even be limited in their physiological capability to increase testosterone levels, which can be tested by injecting birds with gonadotropin-releasing hormone (GnRH). We studied two populations of black redstarts that differ in breeding altitude, morphology and the length of their breeding season. Unexpectedly, males of neither population increased testosterone in response to a simulated territorial intrusion, but injections with GnRH resulted in a major elevation of testosterone. Thus, black redstarts would have been capable of mounting a testosterone response during the male–male Challenge. Our data show, for the first time, that the absence of an androgen response to male–male Challenges is not owing to physiological limitations to increase testosterone. Furthermore, in contrast to comparative evidence between species, populations of black redstarts with a long breeding season do not show the expected elevation in testosterone during male–male Challenges.
Rui Filipe Oliveira - One of the best experts on this subject based on the ideXlab platform.
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Rising to the Challenge? Inter-individual variation of the androgen response to social interactions in cichlid fish.
Hormones and Behavior, 2020Co-Authors: Ana Félix, António Roleira, Rui Filipe OliveiraAbstract:Abstract The Challenge Hypothesis (Wingfield et al. Am. Nat. 136, 829-846) aims to explain the complex relationship between androgens and social interactions. Despite its well acceptance in the behavioral endocrinology literature, several studies have failed to found an androgen response to staged social interactions. Possible reasons for these inconsistencies are the use of single sampling points that may miss the response peak, and the occurrence of inter-individual variability in the androgen response to social interactions. In this study we addressed these two possible confounding factors by characterizing the temporal pattern of the androgen response to social interactions in the African cichlid, Oreochromis mossambicus, and relating it to inter-individual variation in terms of the individual scope for androgen response (i.e. the difference between baseline and maximum physiological levels for each fish) and behavioral types. We found that the androgen response to territorial intrusions varies between individuals and is related to their scope for response. Individuals that have a lower scope for androgen response did not increase androgens after a territorial intrusion but were more aggressive and exploratory. In contrast males with a higher scope for response had fewer aggressive and exploratory behaviors and exhibited two peaks of KT, an early response 2–15 min after the interaction and a late response at 60–90 min post-interaction. Given that the pharmacological Challenge of the Hypothalamic-Pituitary-Gonad axis only elicits the late response, we suggest that these two peaks may be regulated by different physiological mechanisms, with the early response being mediated by direct brain-gonad neural pathways. In summary, we suggest that determining the temporal pattern of the androgen response to social interactions and considering inter-individual variation may be the key to understanding the contradictory results of the Challenge Hypothesis.
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Androgen modulation of social decision-making mechanisms in the brain: an integrative and embodied perspective
Frontiers in Neuroscience, 2014Co-Authors: Gonçalo A. Oliveira, Rui Filipe OliveiraAbstract:Apart from their role in reproduction androgens also respond to social Challenges and this response has been seen as a way to regulate the expression of behaviour according to the perceived social environment (Challenge Hypothesis, Wingfield et al. 1990). This Hypothesis implies that social decision-making mechanisms localized in the central nervous system (CNS) are open to the influence of peripheral hormones that ultimately are under the control of the CNS through the hypothalamic-pituitary-gonadal axis. Therefore, two puzzling questions emerge at two different levels of biological analysis: (1) Why does the brain, which perceives the social environment and regulates androgen production in the gonad, need feedback information from the gonad to adjust its social decision-making processes? (2) How does the brain regulate gonadal androgen responses to social Challenges and how do these feedback into the brain? In this paper, we will address these two questions using the integrative approach proposed by Niko Tinbergen, who proposed that a full understanding of behaviour requires its analysis at both proximate (physiology, ontogeny) and ultimate (ecology, evolution) levels.
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Social instability promotes hormone–behavior associated patterns in a cichlid fish
Hormones and Behavior, 2014Co-Authors: Olinda Almeida, Eliane Gonçalves-de-freitas, Joao S. Lopes, Rui Filipe OliveiraAbstract:Abstract Androgens are known to respond to social Challenges and to control the expression of social behavior and reproductive traits, such as gonadal maturation and sperm production, expression of secondary sex characters and reproductive behaviors. According to the Challenge Hypothesis variation in androgen levels above a breeding baseline should be explained by the regime of social Challenges faced by the individual considering the trade-offs of androgens with other traits (e.g. parental care). One prediction that can be derived from the Challenge Hypothesis is that androgen levels should increase in response to social instability. Moreover, considering that a tighter association of relevant traits is expected in periods of environmental instability, we also predict that in unstable environments the degree of correlations among different behaviors should increase and hormones and behavior should be associated. These predictions were tested in a polygamous cichlid fish (Mozambique tilapia, Oreochromis mossambicus) with exclusive maternal care. Social instability was produced by swapping dominant males among groups. Stable treatment consisted in removing and placing back dominant males in the same group, in order to control for handling stress. Cortisol levels were also measured to monitor stress levels involved in the procedure and their relation to the androgen patterns and behavior. As predicted androgen levels increased in males in response to the establishment of a social hierarchy and presence of receptive females. However, there were no further differential increases in androgen levels over the social manipulation phase between social stable and social unstable groups. As predicted behaviors were significantly more correlated among themselves in the unstable than in the stable treatment and an associated hormone–behavior pattern was only observed in the unstable treatment.
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social modulation of androgens in male vertebrates meta analyses of the Challenge Hypothesis
Animal Behaviour, 2006Co-Authors: Katharina Hirschenhauser, Rui Filipe OliveiraAbstract:The Challenge Hypothesis (Wingfield et al. 1990, American Naturalist, 136, 829–846) predicts varying androgen responses to mating, breeding or territorial behaviour in avian males. At the interspecific level, the highest androgen responsiveness has been observed in males from monogamous species with paternal incubation, and the lowest in males from promiscuous, nonpaternal species. Studies of a number of vertebrate species have discussed the extension of the Challenge Hypothesis predictions to nonavian vertebrates, but a general ‘vertebrate consensus’ has not been achieved. For this quantitative review we included data from all vertebrate species available in the literature into several meta-analyses. We distinguished between the effects of androgens on sexual, aggressive and paternal behaviour and the effects of behaviour on androgen levels and compared these effects between taxa, mating systems and types of parental care. We observed large variations between taxa in all data sets. Nevertheless, at the vertebrate level the Challenge Hypothesis predictions originating from the avian literature were confirmed for the modulation of androgen responsiveness (1) to sexual behaviour by paternal care but not by mating system, and (2) to paternal behaviour by mating system but not the degree of paternal care. In contrast, our results provide (3) no support for the predicted modulation of androgen levels in response to agonistic interactions by mating and parental care system at the vertebrate level. Furthermore, our meta-analyses suggest that the effects of exogenous testosterone on sexual and agonistic behaviour, as a rule of thumb, may be expected to be larger in nonpaternal than in paternal systems.
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a test of the Challenge Hypothesis in cichlid fish simulated partner and territory intruder experiments
Animal Behaviour, 2004Co-Authors: Katharina Hirschenhauser, Michael Taborsky, Tânia Sofia Ferreira De Oliveira, Adelino V M Canario, Rui Filipe OliveiraAbstract:In male birds, the responsiveness of androgens to sexual and territorial behaviour is predicted to vary with mating system and the degree of paternal investment (‘Challenge Hypothesis’, CH; Wingfield et al. 1990, American Naturalist, 136, 829–846). The CH predicts a higher and longer lasting ‘breeding baseline’ androgen level in males of polygynous species with no or only short-term paternal investment than in males of monogamous species with a high degree of paternal investment. Since the applicability of the CH to nonavian vertebrates has been unclear, we experimentally tested its predictions in several cichlid fish (Neolamprologus pulcher, Lamprologus callipterus, Tropheus moorii, Pseudosimochromis curvifrons and Oreochromis mossambicus) using a simulated territorial intruder protocol. Androgens (11-ketotestosterone: 11-KT; testosterone: T) were measured from fish-holding water. In all species sampled, the 11-KT patterns confirmed the predictions of the CH originating from the avian literature, but T patterns did not. Males of all species sampled were highly responsive to territorial intrusions; however, the magnitude and duration of this response, that is, the rapid return to baseline 11-KT levels, could not clearly be explained by the degree of paternal care. 11-KT responses to interactions with ovulating females were observed in maternal mouthbrooders but not in biparental species (e.g. Lamprologini). At the interspecific level, androgen responsiveness was greater among males of monogamous species, as predicted, but also in species with more intense pair bonding (e.g. Tropheus moorii). Thus, this study confirms the predictions of the CH in cichlid fish at both the intraspecific and the interspecific levels.
Ignacio T Moore - One of the best experts on this subject based on the ideXlab platform.
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Testosterone, Territoriality, and Social Interactions in Neotropical Birds
Sexual Selection, 2020Co-Authors: John C Wingfield, Rodrigo A. Vásquez, Ignacio T MooreAbstract:Abstract Our understanding of hormone–behavior relationships is largely based on studies of northern latitude species. Such studies have greatly expanded our general knowledge of the role of testosterone in free-living animals, particularly birds. Results from such studies have resulted in the development of the Challenge Hypothesis, which posits that testosterone levels rise above those necessary for reproduction due to social interactions. However, the vast majority of animals inhabit the tropics and have very different life histories as a consequence. In fact, many southern latitude species have life histories more like tropical species than like their counterparts from northern latitudes. The broad applicability of the findings based on northern species is thus questionable. Based on the few studies of neotropical birds, it appears testosterone and its role in reproduction and social interactions are very different from northern species. Testosterone levels do not elevate in response to male–male interactions, and blocking testosterone does not suppress territorial intrusions. Further studies of both tropical and southern latitude species are thus warranted to develop a broader and deeper understanding of testosterone and its role in reproduction and associated territorial aggression.
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who rises to the Challenge testing the Challenge Hypothesis in fish amphibians reptiles and mammals
Hormones and Behavior, 2020Co-Authors: Ignacio T Moore, Jessica Hernandez, Wolfgang GoymannAbstract:Abstract According to the Challenge Hypothesis, social interactions, particularly among males, have a strong influence on circulating androgen levels. Specifically, males should respond to social Challenges from conspecific males with a rapid increase in plasma androgen levels which support and stimulate further aggression. This basic tenet of the Challenge Hypothesis, an androgen increase in response to a social Challenge from another male, has been tested in all vertebrate classes. While early studies generally supported the Challenge Hypothesis, more recent work has noted numerous exceptions, particularly in birds. Here, we conduct a meta-analysis of studies in fish, amphibians, non-avian reptiles, and mammals that test the prediction that circulating androgen levels of males should increase in response to an experimental Challenge from another male. We found that teleost fish often increase androgens during such Challenges, but other vertebrate groups show more mixed results. Why should fish be different from the other taxa? In fish with paternal care of young, the potential conflict between mating, being aggressive towards other males, and taking care of offspring is alleviated, because females typically choose males based on their defense of an already existing nest. Hence, rather than regulating the trade-off between mating, aggression, and parenting, androgens may have been co-opted to promote all three behaviors. For other taxa, increasing androgen levels only makes sense when the increase directly enhances reproductive success. Thus, the increase in androgen levels is a response to mating opportunities rather than a response to Challenge from another male. To further our understanding of the role of a change in androgen levels in mediating behavioral decision-making between mating, aggression, and parenting, we need studies that address the behavioral consequences of an increase in androgens after male-male encounters and studies that test the androgen responsiveness of species that differ in the degree of paternal care.
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Hormonal response of male green anole lizards (Anolis carolinensis) to GnRH Challenge.
Journal of Experimental Zoology, 2009Co-Authors: Jerry F. Husak, Duncan J. Irschick, Justin P. Henningsen, Kimberly S. Kirkbride, Simon P. Lailvaux, Ignacio T MooreAbstract:Circulating plasma levels of testosterone often differ among social classes of sexually mature males within a population, but the general physiological mechanisms underlying such differences remain unclear. Within sexually mature male green anole lizards (Anolis carolinensis), smaller ''lightweight'' males have on average relatively smaller heads, lower bite- forces, and lower testosterone levels compared with larger ''heavyweight'' males. We conducted gonadotropin-releasing hormone (GnRH) Challenges on lightweight and heavyweight males to determine if lightweight males were capable of producing comparable levels of circulating testosterone to heavyweight males but are socially or physiologically suppressed from doing so. We Challenged lightweight and heavyweight males with chicken I and II GnRH and measured their resulting levels of testosterone and corticosterone. Neither lightweights nor heavyweights increased circulating testosterone levels after GnRH Challenge, suggesting they are already at maximal production levels, consistent with the Challenge Hypothesis. Instead, testosterone levels tended to decrease and corticosterone levels increased, most likely owing to the stress response associated with handling. Our results are dramatically different from GnRH Challenges conducted in bird species, suggesting that more field studies are needed in reptilian systems. J. Exp. Zool. 311A:105-114, 2009. r 2008 Wiley-Liss, Inc.
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Territoriality and testosterone in an equatorial population of rufous-collared sparrows, Zonotrichia capensis
Animal Behaviour, 2004Co-Authors: Ignacio T Moore, Haruka Wada, Nicole Perfito, D. Shallin Busch, Thomas P. Hahn, John C WingfieldAbstract:Territorial aggression, displayed by male vertebrates in a reproductive context, is generally thought to be mediated by testosterone. The Challenge Hypothesis predicts that in socially monogamous species, territorial Challenges should induce an increase in plasma testosterone concentrations, which will enhance aggressive behaviour and territory defence. This Hypothesis is based on northern latitude birds and needs to be tested in tropical birds before it can be universally accepted. We tested the Challenge Hypothesis in an equatorial population of rufous-collared sparrows in Papallacta, Ecuador. This population shows an extended breeding period during which males aggressively guard territories. During the early breeding season, males were Challenged with conspecific or heterospecific simulated territorial intrusions (STIs) lasting 10 min. Conspecific-Challenged males responded more aggressively than heterospecific-Challenged males. However, there was no increase in plasma testosterone in response to the conspecific STI. During the breeding season, males were Challenged with conspecific STIs lasting 0, 10 or 30 min. Males behaved aggressively regardless of STI duration, and did not differ in plasma testosterone or luteinizing hormone concentrations. During the breeding season, males were implanted with testosterone-filled or empty silastic tubes and subsequently Challenged with a conspecific STI. Testosterone implants significantly raised plasma testosterone concentrations, but testosterone-implanted males were not more aggressive than blank-implanted controls. Combined, these findings suggest that testosterone concentrations above breeding baseline are not related to territorial aggression in this population and therefore do not support the Challenge Hypothesis.
Gregory F Ball - One of the best experts on this subject based on the ideXlab platform.
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whither the Challenge Hypothesis
Hormones and Behavior, 2020Co-Authors: John C Wingfield, Marilyn Ramenofsky, Robert E Hegner, Gregory F BallAbstract:Abstract Almost fifty years ago the advent of assay methods to measure circulating levels of hormones revolutionized endocrinology in relation to investigations of free-living and captive animals. This new field “environmental endocrinology” revealed that endocrine profiles in animals in their natural habitat were not only different from captive animals, but often deviated from predictions. It quickly became apparent that the organization and analysis of data from the field should be sorted by life history stages such as for reproductive processes, migration, molt etc. and spaced in time according to natural duration of those processes. Presentation of data by calendar date alone gives much simpler, even misleading, patterns. Stage-organized analyses revealed species-specific patterns of hormone secretion and dramatic inter-individual differences. The “Challenge Hypothesis” sparked exploration of these results, which diverged from expectations of hormone-behavior interactions. The Hypothesis led to specific predictions about how the hypothalamo-pituitary-gonad axis, and particularly circulating patterns of testosterone, might respond to social Challenges such as simulated territorial intrusions. Initially, a group of studies on free-living and captive birds played a key role in the formulation of the Hypothesis. Over the decades since, the effects of social Challenge and environmental context on hormonal responses have been tested in all vertebrate taxa, including humans, as well as in insects. Although it is now clear that the Challenge Hypothesis in its original form is simplistic, field and laboratory tests of the Hypothesis have led to other concepts that have become seminal to the development of environmental endocrinology as a field. In this special issue these developments are addressed and examples from many different taxa enrich the emerging concepts, paving the way for investigations using recent technologies for genetic and transcriptome analyses.
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the neuroendocrine integration of environmental information the regulation and action of testosterone and the Challenge Hypothesis
Hormones and Behavior, 2020Co-Authors: Gregory F Ball, Jacques BalthazartAbstract:Abstract The authors of the original Challenge Hypothesis proposed influential hypotheses concerning the relationship between testosterone concentrations in the blood and aggressive social behaviors. Many of the key observations were made in avian species studied in the wild and in captivity. In this review we evaluate some remaining questions about the ideas discussed in the Challenge Hypothesis from a neuroendocrine perspective. For example, a rise in testosterone in response to a social aggressive stimulus might involve complex social information being processed by the brain and an appropriate signal sent to the gonadotrophin-releasing hormone (GnRH) neuronal system. Alternatively, social stimuli could more directly stimulate the testis and testosterone release via sympathetic innervation of the testis though such pathways have not been linked to a response to social behaviors. The social behavior decision network in the brain seems to play a key role in the regulation of aggressive behavior but how sensory information concerning aggressive behaviors is interpreted appropriately, processed by the social decision network and sent to the GnRH system is still not well understood. There are continuing questions about the extensive species variation in whether an increase in testosterone occurs in response to a territorial Challenge, what its function might be and whether increases in testosterone are necessary to activate morphological changes, or the expression of sexual and aggressive behaviors associated with successful reproduction.
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the Challenge Hypothesis theoretical implications for patterns of testosterone secretion mating systems and breeding strategies
The American Naturalist, 1990Co-Authors: John C Wingfield, Robert E Hegner, Alfred M Dufty, Gregory F BallAbstract:A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be wi...