Flexible circuit mechanisms for context-dependent song sequencing

Many sequenced behaviors, including locomotion, reaching, and vocalization, are patterned differently in different contexts, enabling animals to adjust to their current environments. However, how contextual information shapes neural activity to flexibly alter the patterning of actions is not yet understood. Prior work indicates such flexibility could be achieved via parallel motor circuits, with differing sensitivities to sensory context [1, 2, 3]; instead we demonstrate here how a single neural pathway operates in two different regimes dependent on recent sensory history. We leverage the Drosophila song production system [4] to investigate the neural mechanisms that support male song sequence generation in two contexts: near versus far from the female. While previous studies identified several song production neurons [5, 6, 7, 8], how these neurons are organized to mediate song patterning was unknown. We find that male flies sing 'simple' trains of only one syllable or mode far from the female but complex song sequences consisting of alternations between modes when near to her. We characterize the male song circuit from the brain to the ventral nerve cord (VNC), and find that the VNC song pre-motor circuit is shaped by two key computations: mutual inhibition and rebound excitability [9] between nodes driving the two modes of song. Weak sensory input to a direct brain-to-VNC excitatory pathway (via pC2 brain and pIP10 descending neurons) drives simple song far from the female. Strong sensory input to the same pathway enables complex song production via simultaneous recruitment of P1a neuron-mediated disinhibition of the VNC song pre-motor circuit. Thus, proximity to the female effectively unlocks motor circuit dynamics in the correct sensory context. We construct a compact circuit model to demonstrate that these few computations are sufficient to replicate natural context-dependent song dynamics. These results have broad implications for neural population-level models of context-dependent behavior [10] and highlight that canonical circuit motifs [11, 12, 13] can be combined in novel ways to enable circuit flexibility required for dynamic communication.

Effects of domestication on neophobia: A comparison between the domesticated Bengalese finch (Lonchura striata var. domestica) and its wild ancestor, the white-rumped munia (Lonchura striata)

Bengalese finches (Lonchura striata var. domestica) have more complex song traits than their wild ancestors, white-rumped munias (Lonchura striata). Domesticated finches are likely able to allocate more resources to song development rather than allocating resources to mechanisms aimed at coping with predation, which are no longer needed under domesticated conditions. Here, we aimed to examine the effects of changes in selection pressure due to domestication on the behaviour of Bengalese finches and to contemplate the possible evolutionary mechanisms underlying these changes. To do so, we compared neophobic responses to novel-object conditions as an assessment of reactions to potential predators. We studied groups of Bengalese finches and white-rumped munias and found that Bengalese finches were more likely to eat the food provided to them under novel-object conditions. Bengalese finches had a shorter latency time to eat, and this latency time was less affected by the novel object in the case of Bengalese finches compared to white-rumped munias. Therefore, Bengalese finches have reduced neophobic responses due to domestication. The behavioural strategies of white-rumped munias appear to be more suitable for natural environments, which include unpredictable risks, whereas Bengalese finches have likely adapted their behaviour to the conditions of artificial selection.

Transmission of high-frequency vocalizations from hummingbirds living in diverse habitats

Some species of Andean hummingbirds produce high-frequency vocalizations which exceed the vocal range of most birds. They also challenge our understanding of the role of habitat structure in the evolution of vocal signals because these hummingbirds live in strikingly different habitats, ranging from cloud forest to high-altitude grasslands. Although these vocalizations are produced at high frequencies, they exhibit considerable variation in frequency content and temporal structure. The calls of the hummingbirds from the cloud forest are simpler and have a narrow frequency range compared to the complex song of the grasslands hummingbird. We hypothesized that each of the three high-frequency vocalizations is adapted for transmission in their habitat. We characterized the transmission of high-frequency vocal signals in the cloud forest and in the grasslands. All vocalizations attenuated and degraded substantially at short distances, suggesting that they are adapted for short-range communication. The simple vocalizations of the cloud-forest species transmitted better in both environments compared to the complex song of the grasslands hummingbird, probably due to relaxed constraints for high-frequency sounds in open habitats.

TweetyNet: A neural network that enables high-throughput, automated annotation of birdsong

Songbirds have long been studied as a model system of sensory-motor learning. Many analyses of birdsong require time-consuming manual annotation of the individual elements of song, known as syllables or notes. Here we describe the first automated algorithm for birdsong annotation that is applicable to complex song such as canary song. We developed a neural network architecture, “TweetyNet”, that is trained with a small amount of hand-labeled data using supervised learning methods. We first show TweetyNet achieves significantly lower error on Bengalese finch song than a similar method, using less training data, and maintains low error rates across days. Applied to canary song, TweetyNet achieves fully automated annotation of canary song, accurately capturing the complex statistical structure previously discovered in a manually annotated dataset. We conclude that TweetyNet will make it possible to ask a wide range of new questions focused on complex songs where manual annotation was impractical.

Behavioral, morphological, and ecological trait evolution in two clades of New World Sparrows (Aimophila and Peucaea, Passerellidae)

The New World sparrows (Passerellidae) are a large, diverse group of songbirds that vary in morphology, behavior, and ecology. Thus, they are excellent for studying trait evolution in a phylogenetic framework. We examined lability versus conservatism in morphological and behavioral traits in two related clades of sparrows (Aimophila, Peucaea), and assessed whether habitat has played an important role in trait evolution. We first inferred a multi-locus phylogeny which we used to reconstruct ancestral states, and then quantified phylogenetic signal among morphological and behavioral traits in these clades and in New World sparrows more broadly. Behavioral traits have a stronger phylogenetic signal than morphological traits. Specifically, vocal duets and song structure are the most highly conserved traits, and nesting behavior appears to be maintained within clades. Furthermore, we found a strong correlation between open habitat and unpatterned plumage, complex song, and ground nesting. However, even within lineages that share the same habitat type, species vary in nesting, plumage pattern, song complexity, and duetting. Our findings highlight trade-offs between behavior, morphology, and ecology in sparrow diversification.

Bridging the Safavid–Ottoman Divide

In both Persian and Turkish art-music traditions, despite their significant current differences, the musical idiom of the 15th-century Timurid court is regarded as a significant forbear. Late 15th-century theoretical literature, however, refers to regional variations across the Middle East; these were exacerbated by a lack of continuity in Safavid and Ottoman court patronage during the 16th century, resulting in loss of repertoire and eventual replacement. Yet in the late 17th century commonalities between Safavid and Ottoman art-music practices re-emerge. Although not identical, indeed partly divergent, these practices share a core of frequently used modes and rhythmic cycles and use the same structures for complex song-settings; they even have elements of vocal repertoire in common, while certain Ottoman instrumental pieces are labelled ‘Persian’. There is evidence for the maintenance in both traditions of aesthetic constants in the domains of modulatory practice and formal articulation that can be observed much earlier.

Nonlinear changes in selection on a mating display across a continuous thermal gradient

Understanding how animal communication varies across time and space is critical to understanding how animal signals have evolved and how they function. Changes in temperature, which occur across both time and space, can alter both the courtship and mate choice behaviour of ectothermic animals. In this study, we examine the effect of daily thermal variation on courtship and mate choice in the wolf spider Schizocosa floridana , which produces a complex song with vibrations from three distinct body parts. We test the hypothesis that different components of S. floridana' s courtship respond differently to daily changes in temperature and that corresponding mate choice patterns lead to complex, overlapping shifts in selection on the display itself. By manipulating the thermal environment of courting and choosing pairs, we found that several song components increased in production rate with increased temperature, whereas others decreased, or did not respond at all. We also found evidence that selection on courtship shifts with temperature in several ways, with some display components experiencing directional selection at higher temperatures, but not at lower temperatures. Our findings make it clear that understanding the effect of environmental variation on communication is critical to understanding how selection operates on mate choice and how signals, particularly complex signals, evolve.