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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. Forebrain nuclei linked to woodpecker territorial drum displays mirror those that enable vocal learning in songbirds

   https://doi.org/10.1371/journal.pbio.3001751  

   Schuppe, Eric R. ; Cantin, Lindsey ; Chakraborty, Mukta ; Biegler, Matthew T. ; Jarvis, Electra R. ; Chen, Chun-Chun ; Hara, Erina ; Bertelsen, Mads F. ; Witt, Christopher C. ; Jarvis, Erich D. ; et al ( September 2022 , PLOS Biology)

   Townsend, Simon W. (Ed.)

   Vocal learning is thought to have evolved in 3 orders of birds (songbirds, parrots, and hummingbirds), with each showing similar brain regions that have comparable gene expression specializations relative to the surrounding forebrain motor circuitry. Here, we searched for signatures of these same gene expression specializations in previously uncharacterized brains of 7 assumed vocal non-learning bird lineages across the early branches of the avian family tree. Our findings using a conserved marker for the song system found little evidence of specializations in these taxa, except for woodpeckers. Instead, woodpeckers possessed forebrain regions that were anatomically similar to the pallial song nuclei of vocal learning birds. Field studies of free-living downy woodpeckers revealed that these brain nuclei showed increased expression of immediate early genes (IEGs) when males produce their iconic drum displays, the elaborate bill-hammering behavior that individuals use to compete for territories, much like birdsong. However, these specialized areas did not show increased IEG expression with vocalization or flight. We further confirmed that other woodpecker species contain these brain nuclei, suggesting that these brain regions are a common feature of the woodpecker brain. We therefore hypothesize that ancient forebrain nuclei for refined motor control may have given rise to not only the song control systems of vocal learning birds, but also the drumming system of woodpeckers. 

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3. Evolutionary and Biomechanical Basis of Drumming Behavior in Woodpeckers

   https://doi.org/10.3389/fevo.2021.649146  

   Schuppe, Eric R. ; Rutter, Amy R. ; Roberts, Thomas J. ; Fuxjager, Matthew J. ( July 2021 , Frontiers in Ecology and Evolution)

   null (Ed.)

   Understanding how and why behavioral traits diversify during the course of evolution is a longstanding goal of organismal biologists. Historically, this topic is examined from an ecological perspective, where behavioral evolution is thought to occur in response to selection pressures that arise through different social and environmental factors. Yet organismal physiology and biomechanics also play a role in this process by defining the types of behavioral traits that are more or less likely to arise. Our paper explores the interplay between ecological, physiological, and mechanical factors that shape the evolution of an elaborate display in woodpeckers called the drum. Individuals produce this behavior by rapidly hammering their bill on trees in their habitat, and it serves as an aggressive signal during territorial encounters. We describe how different components of the display—namely, speed (bill strikes/beats sec –1 ), length (total number of beats), and rhythm—differentially evolve likely in response to sexual selection by male-male competition, whereas other components of the display appear more evolutionarily static, possibly due to morphological or physiological constraints. We synthesize research related to principles of avian muscle physiology and ecology to guide inferences about the biomechanical basis of woodpecker drumming. Our aim is to introduce the woodpecker as an ideal study system to study the physiological basis of behavioral evolution and how it relates to selection born through different ecological factors. 

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4. 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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5. Testosterone amplifies the negative valence of an agonistic gestural display by exploiting receiver perceptual bias

   https://doi.org/10.1098/rspb.2021.1848  

   Anderson, Nigel K. ; Grabner, Martina ; Mangiamele, Lisa A. ; Preininger, Doris ; Fuxjager, Matthew J. ( November 2021 , Proceedings of the Royal Society B: Biological Sciences)

   Many animals communicate by performing elaborate displays that are incredibly extravagant and wildly bizarre. So, how do these displays evolve? One idea is that innate sensory biases arbitrarily favour the emergence of certain display traits over others, leading to the design of an unusual display. Here, we study how physiological factors associated with signal production influence this process, a topic that has received almost no attention. We focus on a tropical frog, whose males compete for access to females by performing an elaborate waving display. Our results show that sex hormones like testosterone regulate specific display gestures that exploit a highly conserved perceptual system, evolved originally to detect ‘dangerous' stimuli in the environment. Accordingly, testosterone makes certain gestures likely to appear more perilous to rivals during combat. This suggests that hormone action can interact with effects of sensory bias to create an evolutionary optimum that guides how display exaggeration unfolds. 

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