Socially selected ornaments influence hormone titers of signalers and receivers
26 Jul 2016-Proceedings of the National Academy of Sciences of the United States of America (National Acad Sciences)-Vol. 113, Iss: 30, pp 8478-8483
TL;DR: It is shown that wasps with dishonest signals are aggressively punished, and this punishment has lasting effects on the physiology of the dishonest signaler and those they interact with, and interactions between behavioral and physiological costs of dishonesty could play an important role in maintaining honest communication over evolutionary time.
Abstract: Decades of behavioral endocrinology research have shown that hormones and behavior have a bidirectional relationship; hormones both influence and respond to social behavior. In contrast, hormones are often thought to have a unidirectional relationship with ornaments. Hormones influence ornament development, but little empirical work has tested how ornaments influence hormones throughout life. Here, we experimentally alter a visual signal of fighting ability in Polistes dominulus paper wasps and measure the behavioral and hormonal consequences of signal alteration in signalers and receivers. We find wasps that signal inaccurately high fighting ability receive more aggression than controls and receiving aggression reduces juvenile hormone (JH) titers. As a result, immediately after contests, inaccurate signalers have lower JH titers than controls. Ornaments also directly influence rival JH titers. Three hours after contests, wasps who interacted with rivals signaling high fighting ability have higher JH titers than wasps who interacted with rivals signaling low fighting ability. Therefore, ornaments influence hormone titers of both signalers and receivers. We demonstrate that relationships between hormones and ornaments are flexible and bidirectional rather than static and unidirectional. Dynamic relationships among ornaments, behavior, and physiology may be an important, but overlooked factor in the evolution of honest communication.
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TL;DR: In this paper, the authors survey the literature on different types of costs, focusing in particular on case studies from a diversity of taxa and find that signals often do carry significant physiological production costs, but this is not universal, as many signals appear to be physiologically inexpensive to produce.
34 citations
Cites background from "Socially selected ornaments influen..."
...Contests in this system also affect titres of juvenile hormone in individuals of both high and low quality (Tibbetts et al., 2016), with individuals manipulated to inaccurately signal high quality having reduced titres of juvenile hormone after social interactions....
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TL;DR: In this article, the authors imposed stressful conditions on female tree swallows (Tachycineta bicolor) by attaching groups of feathers during incubation to decrease flight efficiency and maneuverability.
Abstract:
Theory suggests that signal honesty may be maintained by differential costs for high and low quality individuals. For signals that mediate social interactions, costs can arise from the way that a signal changes the subsequent social environment via receiver responses. These receiver-dependent costs may be linked with individual quality through variation in resilience to environmental and social stress. Here, we imposed stressful conditions on female tree swallows (Tachycineta bicolor) by attaching groups of feathers during incubation to decrease flight efficiency and maneuverability. We simultaneously monitored social interactions using an RFID network that allowed us to track the identity of every individual that visited each nest for the entire season. Before treatments, plumage coloration was correlated with baseline and stress-induced corticosterone. Relative to controls, experimentally challenged females were more likely to abandon their nest during incubation. Overall, females with brighter white breasts were less likely to abandon, but this pattern was only significant under stressful conditions. In addition to being more resilient, brighter females received more unique visitors at their nest-box and tended to make more visits to other active nests. In contrast, dorsal coloration did not reliably predict abandonment or social interactions. Taken together, our results suggest that females differ in their resilience to stress and that these differences are signaled by plumage brightness, which is in turn correlated with the frequency of social interactions. While we do not document direct costs of social interaction, our results are consistent with models of signal honesty based on receiver-dependent costs.
32 citations
TL;DR: This perspective piece is the product of a “stock-taking” workshop on sexual selection and sexual conflict and proposes that efforts to resolve four themes can catalyze conceptual progress in the field of sexual selection.
Abstract: In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of ...
25 citations
TL;DR: The challenge hypothesis provides a useful conceptual framework for hypothesis-driven research in insect endocrinology and compares vertebrates and insects provides insight into how selection has shaped patterns of hormone responsiveness as well as the generality of hypotheses originally developed for vertebrates.
16 citations
TL;DR: Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased, suggesting that dominants aggressively punished subordinates who attempted to maintain high fertility.
Abstract: In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones in Polistes dominula paper wasps. Polistes dominula queens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediates Polistes fertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.
16 citations
References
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TL;DR: A phenomenological model is presented, operating on an intraspecific level, which views the cost of secondary sexual development from an endocrinological perspective and proposes a negative-feedback loop between signal intensity and parasite burden by suggesting that testosterone-dependent signal intensity is a plastic response.
Abstract: It has been argued that females should be able to choose parasite-resistant mates on the basis of the quality of male secondary sexual characters and that such signals must be costly handicaps in order to evolve. To a large extent, handicap hypotheses have relied on energetic explanations for these costs. Here, we have presented a phenomenological model, operating on an intraspecific level, which views the cost of secondary sexual development from an endocrinological perspective. The primary androgenic hormone, testosterone, has a dualistic effect; it stimulates development of characteristics used in sexual selection while reducing immu- nocompetence. This "double-edged sword" creates a physiological trade-off that influences and is influenced by parasite burden. We propose a negative-feedback loop between signal intensity and parasite burden by suggesting that testosterone-dependent signal intensity is a plastic re- sponse. This response is modified in accordance with the competing demands of the potential costs of parasite infection versus that of increased reproductive success afforded by exaggerated signals. We clarify how this trade-off is intimately involved in the evolution of secondary sexual characteristics and how it may explain some of the equivocal empirical results that have surfaced in attempts to quantify parasite's effect on sexual selection.
2,595 citations
"Socially selected ornaments influen..." refers background in this paper
...For example, the immunocompetence handicap hypothesis proposes that high androgen titers are required for animals to develop elaborate ornaments and high androgen titers also impose immune-related costs (2, 3)....
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TL;DR: This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions.
Abstract: 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...
2,098 citations
"Socially selected ornaments influen..." refers background in this paper
...Social behavior, in turn, influences hormone titers (15)....
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...Although links between aggression and hormones are common (15), hormone/ behavior links are context dependent and can easily be obscured by other factors (8, 18)....
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TL;DR: A meta-analysis found a significant suppressive effect of testosterone on immunity, in support of the hypothesis, but this effect disappeared when the authors controlled for multiple studies on the same species, and a funnel analysis indicated that the results were robust to a publication bias.
670 citations
"Socially selected ornaments influen..." refers background in this paper
...For example, the immunocompetence handicap hypothesis proposes that high androgen titers are required for animals to develop elaborate ornaments and high androgen titers also impose immune-related costs (2, 3)....
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Book•
07 Aug 2005
TL;DR: This book is a guide to these fascinating connections between animal social behavior and steroid and peptide hormones--a synthesis designed to make it easier for graduate students and researchers to appreciate the excitement, engage in such integrative thinking, and understand the primary literature.
Abstract: Research into the lives of animals in their natural environments has revealed a rich tapestry of complex social relationships and previously unsuspected social and mating systems. The evolution of this behavior is increasingly well understood. At the same time, laboratory scientists have made significant discoveries about how steroid and peptide hormones act on the nervous system to shape behavior. An exciting and rapidly progressing hybrid zone has developed in which these two fields are integrated, providing a fuller understanding of social behavior and the adaptive functions of hormones. This book is a guide to these fascinating connections between animal social behavior and steroid and peptide hormones--a synthesis designed to make it easier for graduate students and researchers to appreciate the excitement, engage in such integrative thinking, and understand the primary literature. Throughout, Elizabeth Adkins-Regan emphasizes concepts and principles, hypothesis testing, and critical thinking. She raises unanswered questions, providing an unparalleled source of ideas for future research. The chapter sequence is by levels of biological organization, beginning with the behavior and hormones of individuals, proceeding to social relationships and systems, and from there to development, behavioral evolution over relatively short time scales, life histories and their evolution, and finally evolution over longer time scales. The book features studies of a wide variety of wild and domestic vertebrates along with some of the most important invertebrate discoveries.
554 citations
TL;DR: The physiological (endocrine) mechanisms that underlie optimal allocation rules and how such rules evolve are discussed and micro‐evolutionary experiments to unravel the mechanistic basis of life‐history evolution are suggested.
Abstract: Summary The negative co-variation of life-history traits such as fecundity and lifespan across species suggests the existence of ubiquitous trade-offs. Mechanistically, trade-offs result from the need to differentially allocate limited resources to traits like reproduction versus selfmaintenance, with selection favoring the evolution of optimal allocation mechanism. Here I discuss the physiological (endocrine) mechanisms that underlie optimal allocation rules and how such rules evolve. The hormone testosteronemaymediatelife-historytrade-offsduetoits pleiotropic actions in male vertebrates. Conservation in the actions of testosterone in vertebrates has prompted the ‘evolutionary constraint hypothesis,’ which assumes that testosterone signaling mechanisms and male traits evolve as a unit. This hypothesis implies that the actions of testosterone are similar across sexes and species, and only the levels of circulating testosterone concentrations change during evolution. In contrast, the ‘evolutionary potential hypothesis’ proposes that testosterone signaling mechanisms and male traits evolve independently. In the latter scenario, the linkage between hormone and traits itself can be shaped by selection, leading to variation in trade-off functions. I will review recent case studies supporting the evolutionary potential hypothesis and suggest micro-evolutionary experiments to unravel the mechanistic basis of lifehistory evolution. BioEssays 29:133–144, 2007. 2007 Wiley Periodicals, Inc.
509 citations
"Socially selected ornaments influen..." refers background in this paper
...” Instead, they are more like flexible “phenotypic integrators” (6) that change in response to the social environment and regulate expression of behavior, morphology, and physiology to match phenotype to the environment (6)....
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