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The long‐distance migrations of thousands of bird species and their billions of individuals are feats of astounding physiological specialization and plasticity. Whereas numerous organ systems require modification to achieve successful fueling and navigation capabilities, given their overarching importance for movement and contribution to body mass, skeletal muscles are subject to exceptional performance optimization and anatomical plasticity. To express the appropriate changes throughout the complicated life history of migration, while remaining in synchrony with the environment, skeletal muscles must receive preparatory signals and express transcriptional and biochemical modifications required for full expression of the migratory phenotype. In all likelihood, these muscles must also temporally signal their state and needs to other organ systems. By considering other well‐studied avian skeletal muscle systems, this review explores how endocrine signaling likely impacts skeletal muscles involved in migration and, conversely, how those muscles might relay their condition elsewhere throughout the bird's body. Systems biology offers exceptional modeling for capturing this complex 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. 

Negotiating social dynamics among allies and enemies is a complex problem that often requires individuals to tailor their behavioral approach to a specific situation based on environmental and/or social factors. One way to make these contextual adjustments is by arranging behavioral output into intentional patterns. Yet, few studies explore how behavioral patterns vary across a wide range of contexts, or how allies might interlace their behavior to produce a coordinated response. Here, we investigate the possibility that resident female and male downy woodpeckers guard their breeding territories from conspecific intruders by deploying defensive behavior in context-specific patterns. To study whether this is the case, we use correlation networks to reveal how suites of agonistic behavior are interrelated. We find that residents do organize their defense into definable patterns, with female and male social mates deploying their behaviors non-randomly in a correlated fashion. We then employ spectral clustering analyses to further distill these responses into distinct behavioral motifs. Our results show that this population of woodpeckers adjusts the defensive motifs deployed according to threat context. When we combine this approach with behavioral transition analyses, our results reveal that pair coordination is a common feature of territory defense in this species. However, if simulated intruders are less threatening, residents are more likely to defend solo, where only one bird deploys defensive behaviors. Overall, our study supports the hypothesis that nonhuman animals can pattern their behavior in a strategic and coordinated manner, while demonstrating the power of systems approaches for analyzing multiagent behavioral dynamics. 

Sexual selection drives the evolution of many spectacular animal displays that we see in nature. Yet, how selection combines and elaborates different signal traits remains unclear. Here, we investigate this issue by testing for correlated evolution between head plumage colour and drumming behaviour in woodpeckers. These signals function in the context of mate choice and male–male competition, and they may appear to a receiver as a single multimodal display. We test for such correlations in males of 132 species using phylogenetic linear models, while considering the effect of habitat. We find that the plumage chromatic contrast is positively correlated with the speed of the drum, supporting the idea that species evolving more conspicuous plumage on their head also evolve faster drum displays. By contrast, we do not find evidence of correlated evolution between drum speed and head colour diversity, size of the head's red patch, or extent of the plumage achromatic contrast. Drum length was not correlated with any of the plumage coloration metrics. Lastly, we find no evidence that habitat acts as a strong selective force driving the evolution of head coloration or drumming elaboration. Coevolution between different signal modalities is therefore complex, and probably depends on the display components in question. 

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. 

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. 

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.