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1. Androgenic modulation of extraordinary muscle speed creates a performance trade-off with endurance

   https://doi.org/10.1242/jeb.222984  

   Tobiansky, Daniel J.; Miles, Meredith C.; Goller, Franz; Fuxjager, Matthew J. (January 2020, Journal of Experimental Biology)

   null (Ed.)

   Performance trade-offs can dramatically alter an organism's evolutionary trajectory by making certain phenotypic outcomes unattainable. Understanding how these trade-offs arise from an animal's design is therefore an important goal of biology. To explore this topic, we study how androgenic hormones, which regulate skeletal muscle function, influence performance trade-offs relevant to different components of complex reproductive behaviour. We conduct this work in golden-collared manakins (Manacus vitellinus), a Neotropical bird in which males court females by rapidly snapping their wings together above their back. Androgens help mediate the snap displays by radically increasing the twitch speed of a dorsal wing muscle [scapulohumeralis caudalis (SH)], which actuates the bird's wing-snap. Through hormone manipulations and in situ muscle recordings, we test how these positive effects on SH speed influence trade-offs with endurance. Indeed, this trait impacts the display by shaping signal length. We find that androgen-dependent increases in SH speed incur a cost to endurance, particularly when this muscle performs at its functional limits. Moreover, when behavioural data are overlaid on our muscle recordings, displaying animals appear to balance display speed with fatigue-induced muscle fusion (physiological tetanus) to generate the fastest possible signal while maintaining an appropriate signal duration. Our results point to androgenic hormone action as a functional trigger of trade-offs in sexual performance—they enhance one element of a courtship display, but in doing so, impede another. 

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2. Specialized androgen synthesis in skeletal muscles that actuate elaborate social displays

   https://doi.org/10.1242/jeb.243730  

   Schuppe, Eric R.; Tobiansky, Daniel; Goller, Franz; Fuxjager, Matthew J. (June 2022, Journal of Experimental Biology)

   ABSTRACT Androgens mediate the expression of many reproductive behaviors, including the elaborate displays used to navigate courtship and territorial interactions. In some vertebrates, males can produce androgen-dependent sexual behavior even when levels of testosterone are low in the bloodstream. One idea is that select tissues make their own androgens from scratch to support behavioral performance. We first studied this phenomenon in the skeletal muscles that actuate elaborate sociosexual displays in downy woodpeckers and two songbirds. We show that the woodpecker display muscle maintains elevated testosterone when the testes are regressed in the non-breeding season. Both the display muscles of woodpeckers, as well as the display muscles in the avian vocal organ (syrinx) of songbirds, express all transporters and enzymes necessary to convert cholesterol into bioactive androgens locally. In a final analysis, we broadened our study by looking for these same transporters and enzymes in mammalian muscles that operate at different speeds. Using RNA-seq data, we found that the capacity for de novo synthesis is only present in ‘superfast’ extraocular muscle. Together, our results suggest that skeletal muscle specialized to generate extraordinary twitch times and/or extremely rapid contractile speeds may depend on androgenic hormones produced locally within the muscle itself. Our study therefore uncovers an important dimension of androgenic regulation of behavior. 

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3. Proposing a neural framework for the evolution of elaborate courtship displays

   https://doi.org/10.7554/eLife.74860  

   Schwark, Ryan W; Fuxjager, Matthew J; Schmidt, Marc F (May 2022, eLife)

   In many vertebrates, courtship occurs through the performance of elaborate behavioral displays that are as spectacular as they are complex. The question of how sexual selection acts upon these animals’ neuromuscular systems to transform a repertoire of pre-existing movements into such remarkable (if not unusual) display routines has received relatively little research attention. This is a surprising gap in knowledge, given that unraveling this extraordinary process is central to understanding the evolution of behavioral diversity and its neural control. In many vertebrates, courtship displays often push the limits of neuromuscular performance, and often in a ritualized manner. These displays can range from songs that require rapid switching between two independently controlled ‘voice boxes’ to precisely choreographed acrobatics. Here, we propose a framework for thinking about how the brain might not only control these displays, but also shape their evolution. Our framework focuses specifically on a major midbrain area, which we view as a likely important node in the orchestration of the complex neural control of behavior used in the courtship process. This area is the periaqueductal grey (PAG), as studies suggest that it is both necessary and sufficient for the production of many instinctive survival behaviors, including courtship vocalizations. Thus, we speculate about why the PAG, as well as its key inputs, might serve as targets of sexual selection for display behavior. In doing so, we attempt to combine core ideas about the neural control of behavior with principles of display evolution. Our intent is to spur research in this area and bring together neurobiologists and behavioral ecologists to more fully understand the role that the brain might play in behavioral innovation and diversification. 

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4. Neck muscle twitch properties are associated with constraint on drum speed in woodpeckers, but not drum length

   https://doi.org/10.1242/jeb.251289  

   Antonson, Nicholas_D; Capano, John_G; Fuxjager, Matthew_J (October 2025, Journal of Experimental Biology)

   Animal displays are often limited by the properties of the muscles that generate them. Here, using in situ muscle stimulation, we investigate the twitch properties of the longus colli ventralis (LCv), a primary muscle used protract the head and neck during territorial drumming displays in woodpeckers. Specifically, we test LCv twitch kinetics and endurance in a manner that simulates drum speed (beats s−1) and length (total beats), two signal feature that can evolve independently of each other. We identify a maximum muscle contraction rate that may represent a physiological constraint relevant to drumming speed, but no relevant constraint on the repetition of contractions that might affect drum length. This suggests twitch properties may differentially affect display components. Broadly, our findings highlight how certain display features may freely diversify independent of others due to physiological limits, while pointing to the way complex signals can evolve under partial performance constraints. 

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5. Layered evolution of gene expression in “superfast” muscles for courtship

   https://doi.org/10.1073/pnas.2119671119  

   Pease, James B.; Driver, Robert J.; de la Cerda, David A.; Day, Lainy B.; Lindsay, Willow R.; Schlinger, Barney A.; Schuppe, Eric R.; Balakrishnan, Christopher N.; Fuxjager, Matthew J. (April 2022, Proceedings of the National Academy of Sciences)

   Identifying the molecular process of complex trait evolution is a core goal of biology. However, pinpointing the specific context and timing of trait-associated changes within the molecular evolutionary history of an organism remains an elusive goal. We study this topic by exploring the molecular basis of elaborate courtship evolution, which represents an extraordinary example of trait innovation. Within the behaviorally diverse radiation of Central and South American manakin birds, species from two separate lineages beat their wings together using specialized “superfast” muscles to generate a “snap” that helps attract mates. Here, we develop an empirical approach to analyze phylogenetic lineage-specific shifts in gene expression in the key snap-performing muscle and then integrate these findings with comparative transcriptomic sequence analysis. We find that rapid wing displays are associated with changes to a wide range of molecular processes that underlie extreme muscle performance, including changes to calcium trafficking, myocyte homeostasis and metabolism, and hormone action. We furthermore show that these changes occur gradually in a layered manner across the species history, wherein which ancestral genetic changes to many of these molecular systems are built upon by later species-specific shifts that likely finalized the process of display performance adaptation. Our study demonstrates the potential for combining phylogenetic modeling of tissue-specific gene expression shifts with phylogenetic analysis of lineage-specific sequence changes to reveal holistic evolutionary histories of complex traits. 

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