Androgen receptor modulates multimodal displays in the Bornean rock frog (Staurois parvus).

Multimodal communication is common in the animal kingdom. It occurs when animals display by stimulating two or more receiver sensory systems, and often arises when selection favors multiple ways to send messages to conspecifics. Mechanisms of multimodal display behavior are poorly understood, particularly with respect to how animals coordinate the production of different signals. One important question is whether all components in a multimodal display share an underlying physiological basis, or whether different components are regulated independently. We investigated the influence of androgen receptors (AR) on the production of both visual and vocal signal components in the multimodal display repertoire of the Bornean rock frog (Staurois parvus). To assess the role of AR in signal production, we treated reproductively active adult males with the antiandrogen flutamide and measured the performance of each signal in the multimodal display. Our results show that blocking AR inhibited the production of multiple visual signals, including a conspicuous visual signal known as the "foot flag," which is produced by rotating the hind limb above the body. However, flutamide treatment caused no measurable change in vocal signaling behavior, or in the frequency or fine temporal properties of males' calls. Our study therefore suggests that activation of AR is not a physiological prerequisite to the coordination of multiple signals, in that it either does not regulate all signaling behaviors in a male's display repertoire or it does so only in a context-dependent manner.

[1]  Aditi Singh,et al.  Conservation and dimorphism in androgen receptor distribution in Alston's singing mouse (Scotinomys teguina) , 2021, The Journal of comparative neurology.

[2]  Meredith C. Miles,et al.  Animal choreography of song and dance: a case study in the Montezuma oropendola, Psarocolius montezuma , 2018, Animal Behaviour.

[3]  Meredith C. Miles,et al.  Macroevolutionary patterning of woodpecker drums reveals how sexual selection elaborates signals under constraint , 2018, Proceedings of the Royal Society B: Biological Sciences.

[4]  Meredith C. Miles,et al.  Androgens Support Male Acrobatic Courtship Behavior by Enhancing Muscle Speed and Easing the Severity of Its Tradeoff With Force , 2017, Endocrinology.

[5]  T. U. Grafe,et al.  Temporal variation in acoustic and visual signalling as a function of stream background noise in the Bornean foot-flagging frog, Staurois parvus , 2017 .

[6]  Meredith C. Miles,et al.  Biogeography predicts macro‐evolutionary patterning of gestural display complexity in a passerine family , 2017, Evolution; international journal of organic evolution.

[7]  Matthew J. Fuxjager,et al.  Insight into the neuroendocrine basis of signal evolution: a case study in foot-flagging frogs , 2017, Journal of Comparative Physiology A.

[8]  Eileen A Hebets,et al.  New dimensions in animal communication: the case for complexity , 2016, Current Opinion in Behavioral Sciences.

[9]  R. S. Taylor,et al.  Increased androgenic sensitivity in the hind limb muscular system marks the evolution of a derived gestural display , 2016, Proceedings of the National Academy of Sciences.

[10]  Matthew J. Fuxjager,et al.  Select forelimb muscles have evolved superfast contractile speed to support acrobatic social displays , 2016, eLife.

[11]  A. Barron,et al.  A systems approach to animal communication , 2016, Proceedings of the Royal Society B: Biological Sciences.

[12]  Matthew J. Fuxjager,et al.  Perspectives on the evolution of animal dancing: a case study of manakins , 2015, Current Opinion in Behavioral Sciences.

[13]  R. Miranda,et al.  Arginine vasotocin induces calling behavior with a female social stimulus and interacts with gonadotropins to affect sexual behaviors in male Xenopus tropicalis , 2015, Physiology & Behavior.

[14]  Matthew J. Fuxjager,et al.  Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor - but not oestrogen receptor - in the forelimb musculature. , 2015, Functional ecology.

[15]  W. Hödl,et al.  From uni- to multimodality: towards an integrative view on anuran communication , 2014, Journal of Comparative Physiology A.

[16]  Matthew J. Fuxjager,et al.  Peripheral androgen action helps modulate vocal production in a suboscine passerine , 2014, The Auk.

[17]  Alistair J. Wilson,et al.  A game theoretic approach to multimodal communication , 2013, Behavioral Ecology and Sociobiology.

[18]  E. Hebets,et al.  An introduction to multimodal communication , 2013, Behavioral Ecology and Sociobiology.

[19]  Matthew J. Fuxjager,et al.  Peripheral androgen receptors sustain the acrobatics and fine motor skill of elaborate male courtship. , 2013, Endocrinology.

[20]  Preston S Wilson,et al.  A bond graph approach to modeling the anuran vocal production system. , 2013, The Journal of the Acoustical Society of America.

[21]  Carolynn L. Smith,et al.  A new heuristic for capturing the complexity of multimodal signals , 2013, Behavioral Ecology and Sociobiology.

[22]  M. Boeckle,et al.  Divergent Receiver Responses to Components of Multimodal Signals in Two Foot-Flagging Frog Species , 2013, PloS one.

[23]  T. U. Grafe,et al.  Multimodal Communication in a Noisy Environment: A Case Study of the Bornean Rock Frog Staurois parvus , 2012, PloS one.

[24]  W. Maddison,et al.  Orchestrating the score: complex multimodal courtship in the Habronattus coecatus group of Habronattus jumping spiders (Araneae: Salticidae) , 2012 .

[25]  D. Kelley,et al.  A neuroendocrine basis for the hierarchical control of frog courtship vocalizations , 2011, Frontiers in Neuroendocrinology.

[26]  Steven M. Phelps,et al.  Androgens modulate song effort and aggression in Neotropical singing mice , 2011, Hormones and Behavior.

[27]  W. Hödl,et al.  The conservation breeding of two foot-flagging frog species from Borneo, Staurois parvus and Staurois guttatus , 2011 .

[28]  Werner Kloas,et al.  Mate calling behavior of male South African clawed frogs (Xenopus laevis) is suppressed by the antiandrogenic endocrine disrupting compound flutamide. , 2010, General and comparative endocrinology.

[29]  J. Bro-Jørgensen Dynamics of multiple signalling systems: animal communication in a world in flux. , 2010, Trends in ecology & evolution.

[30]  Eliot A. Brenowitz,et al.  The Display of the Blue-black Grassquit: The Acoustic Advantage of Getting High , 2010 .

[31]  J. Atwell,et al.  Phenotypic integration and independence: Hormones, performance, and response to environmental change. , 2009, Integrative and comparative biology.

[32]  M. Boeckle,et al.  Communication in Noisy Environments Ii: Visual Signaling Behavior of Male Foot-flagging Frogs staurois Latopalmatus , 2009 .

[33]  M. Boeckle,et al.  Communication in Noisy Environments i: Acoustic Signals of Staurois Latopalmatus Boulenger 1887 , 2009 .

[34]  T. Wanger,et al.  Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling , 2007 .

[35]  D. Kelley,et al.  Direct action of gonadotropin in brain integrates behavioral and reproductive functions , 2007, Proceedings of the National Academy of Sciences.

[36]  B. Schlinger,et al.  Androgen and the elaborate courtship behavior of a tropical lekking bird , 2007, Hormones and Behavior.

[37]  T. Price Phenotypic plasticity, sexual selection and the evolution of colour patterns , 2006, Journal of Experimental Biology.

[38]  D. Kelley,et al.  Historical perspective: Hormonal regulation of behaviors in amphibians , 2005, Hormones and Behavior.

[39]  Kristen A. Potter,et al.  Androgen-induced vocal transformation in adult female African clawed frogs. , 2005, Journal of neurophysiology.

[40]  Sarah R Partan,et al.  Issues in the Classification of Multimodal Communication Signals , 2005, The American Naturalist.

[41]  G. Ball,et al.  Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria) , 2005, Hormones and Behavior.

[42]  E. Hebets Attention-altering Signal Interactions in the Multimodal Courtship Display of the Wolf Spider Schizocosa Uetzi , 2004 .

[43]  Brenton G Cooper,et al.  Multimodal Signals: Enhancement and Constraint of Song Motor Patterns by Visual Display , 2004, Science.

[44]  G. Uetz,et al.  Flexibility in the multi-modal courtship of a wolf spider, Schizocosa ocreata , 2004, Journal of Ethology.

[45]  D. Papaj,et al.  Complex signal function: developing a framework of testable hypotheses , 2004, Behavioral Ecology and Sociobiology.

[46]  Damian O Elias,et al.  Seismic signals in a courting male jumping spider (Araneae: Salticidae) , 2003, Journal of Experimental Biology.

[47]  U. Candolin The use of multiple cues in mate choice , 2003, Biological reviews of the Cambridge Philosophical Society.

[48]  D. Kelley Hormonal Regulation of Motor Output in Amphibians: Xenopus Laevis Vocalizations as a Model System , 2002 .

[49]  W. Wilczynski,et al.  Social Context Influences Androgenic Effects on Calling in the Green Treefrog (Hyla cinerea) , 2001, Hormones and Behavior.

[50]  C. Marler,et al.  The Effects of Arginine Vasotocin on the Calling Behavior of Male Cricket Frogs in Changing Social Contexts , 1998, Hormones and Behavior.

[51]  M. Penna,et al.  Testosterone Levels and Evoked Vocal Responses in a Natural Population of the FrogBatrachyla taeniata , 1997, Hormones and Behavior.

[52]  C. Marler,et al.  Arginine Vasotocin Injection Increases Probability of Calling in Cricket Frogs, but Causes Call Changes Characteristic of Less Aggressive Males , 1995, Hormones and Behavior.

[53]  S. Boyd Arginine Vasotocin Facilitation of Advertisement Calling and Call Phonotaxis in Bullfrogs , 1994, Hormones and Behavior.

[54]  D. Kelley,et al.  Laryngeal muscle and motor neuron plasticity in Xenopus laevis: testicular masculinization of a developing neuromuscular system. , 1993, Journal of neurobiology.

[55]  D. Kelley,et al.  Sexually dimorphic expression of a laryngeal-specific, androgen-regulated myosin heavy chain gene during Xenopus laevis development. , 1992, Developmental biology.

[56]  D. Kelley,et al.  Vocalizations by a sexually dimorphic isolated larynx: peripheral constraints on behavioral expression , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  D. Kelley,et al.  The sexually dimorphic larynx of Xenopus laevis: development and androgen regulation. , 1986, The American journal of anatomy.

[58]  D. Crews,et al.  Evolution of mechanisms controlling mating behavior. , 1986, Science.

[59]  D. Kelley,et al.  Androgen and gonadotropin effects on male mate calls in South African clawed frogs, Xenopus laevis , 1983, Hormones and Behavior.

[60]  W Wickler,et al.  A special constraint on the evolution of composite signals. , 2010, Zeitschrift fur Tierpsychologie.

[61]  M. Wada,et al.  Relation of mode of administration of testosterone to evocation of male sex behavior in frogs , 1977, Hormones and Behavior.

[62]  J. Wingfield,et al.  Correlation between blood level of androgens and sexual behavior in male leopard frogs, Rana pipiens. , 1976, General and comparative endocrinology.