Selection for Rhythm as a Trigger for Recursive Evolution in the Elaborate Display System of Woodpeckers.

Evolution is never truly predictable, in part because the process of selection is recursive: it operates on its own output to generate historical contingencies, so emergent traits can reshape how others evolve in the future. Studies rarely attempt to directly trace how recursion underlies present-day phenotypic pattern on a macroevolutionary basis. To address this gap, we examined how different selection regimes-each operating on a different timescale-guide the evolution of the woodpecker drum display. Approximately 200 species drum with distinctive speed and length, which are important for territorial competition. We discovered remarkable variation in drum rhythm, with some species drumming at constant rates and others changing speed along a range of mathematical functions. Rhythm undergoes divergent character displacement among sympatric sister species, a process that wanes as other reproductive boundaries emerge over time. Tracing the recursive effects of this process, we found that modifying rhythm may then potentiate or constrain speed/length elaboration. Additionally, increased sexual size dimorphism predicts the emergence of rhythms associated with constrained evolutionary rates of speed/length, implying that selection can also constrain itself. Altogether, our findings illustrate how recursion introduces contingencies that allow diverse phenotypes to arise from similar selection regimes.

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

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 studied how androgenic hormones, which regulate skeletal muscle function, influence performance trade-offs relevant to different components of complex reproductive behaviour. We conducted 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 this behavior 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 tested how these positive effects on SH speed influence trade-offs with endurance. Indeed, this latter trait impacts the display by shaping signal length. We found 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 were overlaid on our muscle recordings, displaying animals appeared 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 androgen action as a functional trigger of trade-offs in sexual performance - these hormones enhance one element of a courtship display, but in doing so, impede another.

Phenotypic Diversity Arises from Secondary Signal Loss in the Elaborate Visual Displays of Toucans and Barbets.

Complexity and diversity are fundamental characteristics of life, but the relationship between the two remains murky. For example, both gaining and losing complexity can support diversity-so how exactly does complexity influence the emergence of unique phenotypes? Here we address this question by examining how complexity underlies the diversity of elaborate visual displays in the avian clade Ramphastides (toucans and barbets). These species communicate in part by using body movement and colorful ornaments on the tail. We find that sexual size dimorphism predicts the evolution of one specific signal, the tail-cock gesture, implying that tail cocking is more likely to evolve under stronger sexual selection. We also discover process-level constraints on the evolution of complexity: signals are gained along a strict order of operations, where the tail-cock gesture arises before other colors and gestures. Yet virtually any signal can be lost at any time. As a result, many extant phenotypes were more likely to arise through loss of complexity, highlighting the importance of secondary signal loss to phenotypic diversity. Collectively, our results demonstrate how sexual selection catalyzes the evolution of complex phenotypes, which indirectly support diversity by allowing different traits to be modified or lost in the future.

Macroevolutionary patterning of woodpecker drums reveals how sexual selection elaborates signals under constraint.

Sexual selection drives elaboration in animal displays used for competition and courtship, but this process is opposed by morphological constraints on signal design. How do interactions between selection and constraint shape display evolution? One possibility is that sexual selection continues exaggeration under constraint by operating differentially on each signal component in complex, modular displays. This is seldom studied on a phylogenetic scale, but we address the issue herein by studying macroevolutionary patterning of woodpecker drum displays. These territorial displays are produced when an individual rapidly hits its bill on a hard surface, and drums vary across species in the number of beats included (length) and the rate of drumbeat production (speed). We report that species body size limits drum speed, but not drum length. As a result of this biomechanical constraint, there is less standing variation in speed than length. We also uncover a positive relationship between sexual size dimorphism and the unconstrained trait (length), but with no effect on speed. This suggests that when morphology limits the exaggeration of one component, sexual selection instead exaggerates the unconstrained trait. Modular displays therefore provide the basis for selection to find novel routes to phenotypic elaboration after previous ones are closed.

Evolution of the androgen-induced male phenotype.

The masculine reproductive phenotype varies significantly across vertebrates. As a result, biologists have long recognized that many of the mechanisms that support these phenotypes-particularly the androgenic system-is evolutionarily labile, and thus susceptible to the effects of selection for different traits. However, exactly how androgenic signaling systems vary in a way which results in dramatically different functional outputs, remain largely unclear. We explore this topic here by outlining four key-but non-mutually exclusive-hypotheses that propose how the mechanisms of androgenic signaling might change over time to potentiate the emergence of phenotypical variation in masculine behavior and physiology. We anchor this framework in a review of our own studies of a tropical bird called the golden-collared manakin (Manacus vitellinus), which has evolved an exaggerated acrobatic courtship display that is heavily androgen-dependent. The result is an example of how the cellular basis of androgenic action can be modified to support a unique reproductive repertoire. We end this review by highlighting a broad pathway forward to further pursue the intricate ways by which the mechanisms of hormone action evolve to support processes of adaptation and animal design.

Synergistic selection regimens drive the evolution of display complexity in birds of paradise.

Integrated visual displays that combine gesture with colour are nearly ubiquitous in the animal world, where they are shaped by sexual selection for their role in courtship and competition. However, few studies assess how multiple selection regimens operate on different components of these complex phenotypes on a macroevolutionary scale. Here, we study this issue by assessing how both sexual and ecological selection work together to influence visual display complexity in the birds of paradise. We first find that sexual dichromatism is highest in lekking species, which undergo more intense sexual selection by female choice, than non-lekking species. At the same time, species in which males directly compete with one another at communal display courts have more carotenoid-based ornaments and fewer melanin ornaments. Meanwhile, display habitat influences gestural complexity. Species that dance in the cluttered understorey have more complex dances than canopy-displaying species. Taken together, our results illustrate how distinct selection regimens each operate on individual elements comprising a complex display. This supports a modular model of display evolution, wherein the ultimate integrated display is the product of synergy between multiple factors that select for different types of phenotypic complexity.

Evolution of the androgen receptor: Perspectives from human health to dancing birds.

Androgenic hormones orchestrate the development and activation of diverse reproductive phenotypes across vertebrates. Although extensive work investigates how selection for these traits modifies individual elements of this signaling system (e.g., hormone or androgen receptor [AR] levels), we know less about natural variation in the AR sequence across vertebrates. Our knowledge of AR sequence mutations is largely limited to work in human patients or cell-lines, providing a framework to contextualize single mutations at the expense of evolutionary timescale. Here we unite both perspectives in a review that explores the functional significance of AR on a domain-by-domain basis, using existing knowledge to highlight how and why each region might evolve. We then examine AR sequence variation on different timescales by examining sequence variation in clades originating in the Cambrian (vertebrates; >500 mya) and Cretaceous (birds; >65 mya). In each case, we characterize how the receptor has changed over time and discuss which regions are most likely to evolve in response to selection. Overall, domains that are required for androgenic signaling to function (e.g., DNA- and ligand-binding) tend to be conserved. Meanwhile, areas that interface with co-regulatory molecules can exhibit notable variation even between closely related species. We propose that accumulating mutations in regulatory regions is one way that AR structure might act as a substrate for selection to guide the evolution of reproductive traits. By synthesizing literature across disciplines and highlighting the evolutionary potential of specific AR regions, we hope to inspire new avenues of integrative research into endocrine system evolution.

Physiological constraint on acrobatic courtship behavior underlies rapid sympatric speciation in bearded manakins.

Physiology's role in speciation is poorly understood. Motor systems, for example, are widely thought to shape this process because they can potentiate or constrain the evolution of key traits that help mediate speciation. Previously, we found that Neotropical manakin birds have evolved one of the fastest limb muscles on record to support innovations in acrobatic courtship display (Fuxjager et al., 2016a). Here, we show how this modification played an instrumental role in the sympatric speciation of a manakin genus, illustrating that muscle specializations fostered divergence in courtship display speed, which may generate assortative mating. However, innovations in contraction-relaxation cycling kinetics that underlie rapid muscle performance are also punctuated by a severe speed-endurance trade-off, blocking further exaggeration of display speed. Sexual selection therefore potentiated phenotypic displacement in a trait critical to mate choice, all during an extraordinarily fast species radiation-and in doing so, pushed muscle performance to a new boundary altogether.

Standing Variation and the Capacity for Change: Are Endocrine Phenotypes More Variable Than Other Traits?

Circulating steroid hormone levels exhibit high variation both within and between individuals, leading some to hypothesize that these phenotypes are more variable than other morphological, physiological, and behavioral traits. This should have profound implications for the evolution of steroid signaling systems, but few studies have examined how endocrine variation compares to that of other traits or differs among populations. Here we provide such an analysis by first exploring how variation in three measures of corticosterone (CORT)-baseline, stress-induced, and post-dexamethasone injection-compares to variation in key traits characterizing morphology (wing length, mass), physiology (reactive oxygen metabolite concentration [d-ROMs] and antioxidant capacity), and behavior (provisioning rate) in two populations of tree swallow (Tachycineta bicolor). After controlling for measurement precision and within-individual variation, we found that only post-dex CORT was more variable than all other traits. Both baseline and stress-induced CORT exhibit higher variation than antioxidant capacity and provisioning rate, but not oxidative metabolite levels or wing length. Variation in post-dex CORT and d-ROMs was also elevated in the higher-latitude population in that inhabits a less predictable environment. We next studied how these patterns might play out on a macroevolutionary scale, assessing patterns of variation in baseline testosterone (T) and multiple non-endocrine traits (body length, mass, social display rate, and locomotion rate) across 17 species of Anolis lizards. At the macroevolutionary level, we found that circulating T levels and the rate of social display output are higher than other behavioral and morphological traits. Altogether, our results support the idea that within-population variability in steroid levels is substantial, but not exceptionally higher than many other traits that define animal phenotypes. As such, circulating steroid levels in free-living animals should be considered traits that exhibit similar levels of variability from individual to individual in a population.

Biogeography predicts macro-evolutionary patterning of gestural display complexity in a passerine family.

Gestural displays are incorporated into the signaling repertoire of numerous animal species. These displays range from complex signals that involve impressive and challenging maneuvers, to simpler displays or no gesture at all. The factors that drive this evolution remain largely unclear, and we therefore investigate this issue in New World blackbirds by testing how factors related to a species' geographical distribution and social mating system predict macro-evolutionary patterns of display elaboration. We report that species inhabiting temperate regions produce more complex displays than species living in tropical regions, and we attribute this to (i) ecological factors that increase the competitiveness of the social environment in temperate regions, and (ii) different evolutionary and geological contexts under which species in temperate and tropical regions evolved. Meanwhile, we find no evidence that social mating system predicts species differences in display complexity, which is consistent with the idea that gestural displays evolve independently of social mating system. Together, these results offer some of the first insight into the role played by geographic factors and evolutionary context in the evolution of the remarkable physical displays of birds and other vertebrates.

Androgens Support Male Acrobatic Courtship Behavior by Enhancing Muscle Speed and Easing the Severity of Its Tradeoff With Force.

Steroid hormone action in the brain regulates many animals' elaborate social displays used for courtship and competition, but it is increasingly recognized that the periphery may also be a site for potent steroidal modulation of complex behavior. However, the mechanisms of such "bottom-up" regulation of behavioral outflow are largely unclear. To study this problem, we examined how androgenic sex hormones act through the skeletal muscular system to mediate elaborate courtship acrobatics in a tropical bird called the golden-collared manakin. As part of their display, males snap their wings together above their backs at rates that are at least 2× faster than the normal wing-beat frequency used for flight. This behavior, called the roll-snap, is actuated by repeatedly activating a humeral retractor muscle-the scapulohumeralis caudalis (SH)-which produces contraction-relaxation cycling speeds similar to the "superfast" muscles of other taxa. We report that endogenous androgenic activation of androgen receptor (AR) sustains this muscle's exceptionally rapid contractile kinetics, allowing the tissue to generate distinct wing movements at oscillation frequencies >100 Hz. We also show that these effects are rooted in an AR-dependent increase to contractile velocity, which incurs no detectable cost to force generation. Thus, AR enhances SH speed necessary for courtship display performance while avoiding the expected tradeoff with strength that could otherwise negatively influence aspects of flight. Peripheral AR therefore not only sets up the muscular system to perform a complex wing display, but does so in a way that balances the functional requirements of this muscle for other life-sustaining behavior.