Across diverse organisms, the strength and ecological drivers of sexual selection vary enormously. In birds, some of the families with the most elaborate plumage and display-such as birds of paradise, manakins, and cotingas-are also specialist frugivores, yet links between shifts in diet, changes in breeding system, and the evolution of elaborate traits are poorly understood. We focus on manakins, a radiation of frugivorous Neotropical birds well known for spectacular courtship rituals and colorful plumage, and present an integrative analysis of the transition in both diet and mating systems in this clade to examine the causes and consequences of strong sexual selection. In manakins, we find reduced genetic diversity on the Z sex chromosome relative to autosomes, a predicted signature of sexual selection. We also identify targets of positive selection across the manakin radiation, including genes related to muscle function, visual perception, and the transition to frugivory. Among these, we observe selection on sugar-sensing taste receptors, as well as on lactase-phlorizin hydrolase, implicated in the consumption of chemically defended fruits. For both, we confirm that selection signatures correspond to functional changes and infer the relative time of these changes, as well as of shifts in diet, breeding systems, and plumage coloration: elaborated traits evolved subsequent to changes in mating systems and after key physiological changes facilitating fruit-eating. Altogether, these results suggest that intensified frugivory set the stage for the radiation of one of the planet's most colorful and acrobatic avian lineages.

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.

AbstractAnimals that are successful in urban habitats often have reduced antipredator responses toward people (sometimes called “fear” responses). However, few studies test whether sympatric species differ in their responses to humans, which may explain differing sensitivities to urbanization. Here, we quantified the behavioral and physiological responses to humans in two lizard species, side-blotched lizards (Uta stansburiana) and western fence lizards (Sceloporus occidentalis), across three different habitat types that vary in human impact: natural habitats with low levels of human activity, natural habitats with high levels of human activity, and urban habitats. We found that side-blotched lizards had longer flight initiation distances, were found closer to a refuge, and were more likely to hide than fence lizards, behaviors that could indicate greater fearfulness. Both lizard species were found closer to a refuge and were also more likely to hide in the urban habitat than in the natural habitat with low human impact, which could represent adaptive behaviors for increased risks in urban areas (e.g. cats). Western fence lizards exhibited lower body sizes and conditions in the habitats with moderate and high levels of human activity, whereas these traits did not differ among habitats in side-blotched lizards. Baseline and stress-induced corticosterone concentrations did not differ across habitats for both species, suggesting that human-impacted habitats were not stressful or that lizards had undergone habituation-like processes in these habitats. Taken together, our results highlight the importance of standardized measurements across multiple species in the same habitats to understand differential responses to human-induced environmental change.

Organismal behavior, with its tremendous complexity and diversity, is generated by numerous physiological systems acting in coordination. Understanding how these systems evolve to support differences in behavior within and among species is a longstanding goal in biology that has captured the imagination of researchers who work on a multitude of taxa, including humans. Of particular importance are the physiological determinants of behavioral evolution, which are sometimes overlooked because we lack a robust conceptual framework to study mechanisms underlying adaptation and diversification of behavior. Here, we discuss a framework for such an analysis that applies a "systems view" to our understanding of behavioral control. This approach involves linking separate models that consider behavior and physiology as their own networks into a singular vertically integrated behavioral control system. In doing so, hormones commonly stand out as the links, or edges, among nodes within this system. To ground our discussion, we focus on studies of manakins (Pipridae), a family of Neotropical birds. These species have numerous physiological and endocrine specializations that support their elaborate reproductive displays. As a result, manakins provide a useful example to help imagine and visualize the way systems concepts can inform our appreciation of behavioral evolution. In particular, manakins help clarify how connectedness among physiological systems-which is maintained through endocrine signaling-potentiate and/or constrain the evolution of complex behavior to yield behavioral differences across taxa. Ultimately, we hope this review will continue to stimulate thought, discussion, and the emergence of research focused on integrated phenotypes in behavioral ecology and endocrinology.

Androgens are a class of hormones that bind to androgen receptors (AR) to promote significant changes to cells possessing AR. Testosterone is made more potent by its conversion to 5-dihydrotestosterone (DHT) by the enzyme 5-reductase. Studying the way androgens act on AR receptors in a small wild tropical bird can be challenging. Using a variety of techniques, male golden-collared manakins were found to possess 5-reductase and AR at high levels in spinal motor and sensory neurons, in the brain and in skeletal muscles important for the performance of courtship displays, including wingsnapping. Across a diversity of birds, including several manakins, the amount of androgen receptor in muscle is found to correlate with the complexity of courtship behavior, evidence that androgen action on muscle is key to the physicality of avian courtship behavior.

Basic principles of endocrinology, sex determination, and sexual differentiation underlie many facets of manakin biology: hormones, which, coordinate the functions of multiple organ systems: steroids, which play a special role in regulating reproductive processes, including behavior; tissues, which can be involved in regulating complex molecular events within cells. In some cases, hormonal exposure leads to sex-specific phenotypes. The sexes differentiate early in fetal development based, at least in mammals and birds, on chromosomal composition. Sex-specific chromosomes then guide gonadal development, and the gonads secrete hormones, including steroids, to guide the formation of anatomical features appropriate for the gonad that is present. Some tissues do develop sexual phenotypes independent of hormones likely owing to the action of the sex chromosomes present in cells of that tissue. This latter mechanism is easily observed in birds called gynandromorphs that are laterally sexually dimorphic.

A major goal of evolutionary biology is to understand how sexual traits arise and diversify among populations. One way to address this objective is by studying sexual traits in closely related species and their hybrids. Here, we used this approach to study the evolution of elaborate behavioural display characteristics used during courtship. We focus on bearded manakins (genus: Manacus), where males of this avian clade perform an acrobatic jump-snap display to court females. Hybridization is common among Manacus taxa, and thus, we studied courtship dance behaviour in a hybrid population between golden-collared manakins, Manacus vitellinus, and white-collared manakins, Manacus candei. We found that, despite being genetically more similar to white-collared manakins, hybrid males performed key dance manoeuvres like golden-collared manakins. Hybrids performed other dance manoeuvres intermediate to the two species, or more like their white-collared parents. Select components of the birds' dance routines may have therefore introgressed from the golden-collared population into the white-collared populations. We hypothesize that such modular evolution occurs in response to sexual selection, whereby specific components of the bird's dance routine shift to yield a broader change in its functional appearance.

Over the past few years our understanding of estrogen signaling in the brain has expanded rapidly. Estrogens are synthesized in the periphery and in the brain, acting on multiple receptors to regulate gene transcription, neural function, and behavior. Various estrogen-sensitive signaling pathways often operate in concert within the same cell, increasing the complexity of the system. In females, estrogen concentrations fluctuate over the estrous/menstrual cycle, dynamically modulating estrogen receptor (ER) expression, activity, and trafficking. These dynamic changes influence multiple behaviors but are particularly important for reproduction. Using the female rodent model, we review our current understanding of estradiol signaling in the regulation of sexual receptivity.

Biologists have long been fascinated by the elaborate courtship displays performed by diverse organisms throughout the animal kingdom. The evolution of courtship behaviour often requires specializations of neural, sensory and motor systems. In addition, physically impressive displays may also require optimized metabolic, respiratory and cardiovascular systems to sustain the neuromuscular demands. Hormonal signalling can reach all of these tissues simultaneously to prepare them for use in courtship. Studies of male golden-collared manakins, Manacus vitellinus, a small bird of the Neotropics with a physically intense and noisy courtship display, have uncovered numerous androgen-dependent neuromuscular and metabolic specializations that enable not only the performance of elaborate courtship routines, but also their evolutionary exaggeration. However, physiological specializations for one function can create limits on their use for other purposes. Such trade-offs may influence the way courtship develops but may also provide information used by females for mate choice. We review this body of work with an eye towards expanding our appreciation of the evolution of widespread tissue hormone sensitivity and hormone action as the system through which elaborate courtship behaviours evolve. (c) 2021 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Type 2 diabetes mellitus (T2DM) is associated with abnormal communication among large-scale brain networks, revealed by resting-state functional connectivity (rsFC), with inconsistent results between studies. We performed a meta-analysis of seed-based rsFC studies to identify consistent network connectivity alterations. Thirty-three datasets from 30 studies (1014 T2DM patients and 902 healthy controls [HC]) were included. Seed coordinates and between-group effects were extracted, and the seeds were divided into networks based on their location. Compared to HC, T2DM patients showed hyperconnectivity and hypoconnectivity within the DMN, DMN hypoconnectivity with the affective network (AN), ventral attention network (VAN) and frontal parietal network, and DMN hyperconnectivity with the VAN and visual network. T2DM patients also showed AN hypoconnectivity with the somatomotor network and hyperconnectivity with the VAN. T2DM illness durations negatively correlated with within-DMN rsFC. These DMN-centered impairments in large-scale brain networks in T2DM patients may help to explain the cognitive deficits associated with T2DM.

The zebra finch (Taeniopygia guttata), a representative oscine songbird species, has been widely studied to investigate behavioral neuroscience, most notably the neurobiological basis of vocal learning, a rare trait shared in only a few animal groups including humans. In 2019, an updated zebra finch genome annotation (bTae-Gut1_v1.p) was released from the Ensembl database and is substantially more comprehensive than the first version published in 2010. In this study, we utilized the publicly available RNA-seq data generated from Illumina-based short-reads and PacBio single-molecule real-time (SMRT) long-reads to assess the bird tran-scriptome. To analyze the high-throughput RNA-seq data, we adopted a hybrid bioinformatic approach combining short and long-read pipelines. From our analysis, we added 220 novel genes and 8,134 transcript variants to the Ensembl annotation, and predicted a new proteome based on the refined annotation. We further validated 18 different novel proteins by using mass-spectrometry data generated from zebra finch caudal telencephalon tissue. Our results provide additional resources for future studies of zebra finches utilizing this improved bird genome annotation and proteome.

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.

Regulation of glucocorticoids (GCs), important mediators of physiology and behavior at rest and during stress, is multi-faceted and dynamic. The 11ß hydroxysteroid dehydrogenases 11ß-HSD1 and 11ß-HSD2 catalyze the regeneration and inactivation of GCs, respectively, and provide peripheral and central control over GC actions in mammals. While these enzymes have only recently been investigated in just two songbird species, central expression patterns suggest that they may function differently in birds and mammals, and little is known about how peripheral expression regulates circulating GCs. In this study, we utilized the 11ß-HSD inhibitor carbenoxolone (CBX) to probe the functional effects of 11ß-HSD activity on circulating GCs and central GC-dependent gene expression in the adult zebra finch (Taeniopygia guttata). Peripheral CBX injection produced a marked increase in baseline GCs 60 min after injection, suggestive of a dominant role for 11ß-HSD2 in regulating circulating GCs. In the adult zebra finch brain, where 11ß-HSD2 but not 11ß-HSD1 is expressed, co-incubation of micro-dissected brain regions with CBX and stress-level GCs had no impact on expression of several GC-dependent genes. These results suggest that peripheral 11ß-HSD2 attenuates circulating GCs, whereas central 11ß-HSD2 has little impact on gene expression. Instead, rapid 11ß-HSD2-based regulation of local GC levels might fine-tune membrane GC actions in brain. These results provide new insights into the dynamics of GC secretion and action in this important model organism.

A Correction to this paper has been published: https://doi.org/10.1038/s41586-021-03473-8.

•Behavioral Neuroendocrinology is fast-growing field of research.•Studies investigating animals in nature is expanding and of critical importance.•Multidisciplinary approaches expand our science.•The journal Hormones and Behavior is a foundation of modern research.•Hormones and Behavior must continue multidisciplinary and comparative perspectives.