Notes on a tree: reframing the relevance of primate choruses, duets, and solo songs

The complexity of primates’ singing behavior has long gathered the attention of researchers interested in understanding the selective pressures underpinning the evolution of language. Among these pressures, a link between territoriality, pair-living, and singing displays has been suggested. Historically, singing primates have been found in a few taxa that are not closely related to each other, and, in the last years, their phylogeny has dramatically changed. Hence, we aimed at understanding if the dogmatic association between territorial behavior and a monogamous social structure still holds in the light of current research. Moreover, singing behavior has often been considered a whole, but animals can perform different singing forms depending on how many individuals call simultaneously. Currently, it is unclear to which extent these singing forms are widespread among these primate groups. Given that there is no unique definition for a song, solo, duet, and chorus, we envisioned some of the most used descriptions. We then formulated some new definitions that we followed in our review of the presence/absence of these different forms of song organization among singing primates’ taxa. In particular, we suggested that tarsier species that are typically considered non-singers may indeed sing, and we pointed out that non-duetting gibbons may perform duet interactions. We found that, besides duets, chorusing behavior and solo songs are essential features of primates’ communication, but their study is still in a descriptive phase. Moreover, while territorial behavior seems to be conserved in these singing taxa, we highlighted that the monogamous social structure is not the rule. Pair-living plus multi- females groups displaying singing behavior are common too. We suggest that ending to consider these taxa as uniform in their sociality and vocal behavior might be a significant turning point to unravel the different selective pressures that influenced the emergence and organization of such peculiar vocal behavior.

Cohesion in male singing behavior predicts group reproductive output in a social songbird

All social groups require organization to function optimally. Group organization is often shaped by social 'rules', which function to manage conflict, discourage cheating, or promote cooperation. If social rules promote effective social living, then the ability to learn and follow these rules may be expected to influence individual and group-level fitness. However, such links can rarely be tested, due to the complexity of the factors mediating social systems and the difficulty of gathering data across multiple groups. Songbirds offer an opportunity to investigate the link between social rules and reproductive output because most of their social interactions are mediated by song, a well-studied and readily quantifiable behavior. Using observations from 19 groups of brown-headed cowbirds (Molothrus ater) studied across 15 years, we find evidence for a previously undocumented social rule: cohesive group transitions between dominance- and courtship-related singing. Comparing across groups, the degree of cohesion in male singing behavior predicts the reproductive output of their group. Experimental manipulation of group structure via the introduction of juvenile males to captive flocks reduced group cohesion and adult male reproductive success. Taken together, these results demonstrate that cohesion in group behavioral states can affect both individual and group-level reproductive success, suggesting that selection can act not only on individual-level traits, but also on an individual's ability and opportunity to participate effectively in organized social interactions. Social cohesion could therefore be an unappreciated force affecting social evolution in many diverse systems.

Intrinsic motivation for singing in songbirds is enhanced by temporary singing suppression and regulated by dopamine

Behaviors driven by intrinsic motivation are critical for development and optimization of physical and brain functions, but their underlying mechanisms are not well studied due to the complexity and autonomy of the behavior. Songbirds, such as zebra finches, offer a unique opportunity to study neural substrates of intrinsic motivation because they spontaneously produce many renditions of songs with highly-quantifiable structure for vocal practice, even in the absence of apparent recipients (“undirected singing”). Neural substrates underlying intrinsic motivation for undirected singing are still poorly understood partly because singing motivation cannot be easily manipulated due to its autonomy. Also, undirected singing itself acts as an internal reward, which could increase singing motivation, leading to difficulty in measuring singing motivation independent of singing-associated reward. Here, we report a simple procedure to easily manipulate and quantify intrinsic motivation for undirected singing independent of singing-associated reward. We demonstrate that intrinsic motivation for undirected singing is dramatically enhanced by temporary suppression of singing behavior and the degree of enhancement depends on the duration of suppression. Moreover, by examining latencies to the first song following singing suppression as a measure of singing motivation independent of singing-associated reward, we demonstrate that intrinsic singing motivation is critically regulated by dopamine through D2 receptors. These results provide a simple experimental tool to manipulate and measure the intrinsic motivation for undirected singing and illustrate the importance of zebra finches as a model system to study the neural basis of intrinsically-motivated behaviors.

Singing Fin Whale Swimming Behavior in the Central North Pacific

Male fin whales sing using 20 Hz pulses produced in regular patterns of inter-note intervals, but little is known about fin whale swimming behavior while they are singing. Even less is known about fin whales in Hawaiian waters because they have rarely been sighted during surveys and passive acoustic monitoring has been limited to sparse hydrophone systems that do not have localization capabilities. We hypothesized that fin whale kinematics may be related to their singing behavior, or external variables such as time and sea state. To investigate this hypothesis, we analyzed 115 tracks containing 50,034 unique notes generated from passive acoustic recordings on an array of 14 hydrophones from 2011 to 2017 at the U.S. Navy Pacific Missile Range Facility off Kauai, Hawaii. Fin whales swam at an average speed of 1.1 m/s over relatively direct paths. We incorporated the whales' speed and turning angle into hidden Markov models to identify different behavioral states based on the whales' movements. We found that fin whale kinematic behavioral state was related to the vocalization rate (also known as cue rate) and time of day. When cue rate was higher, fin whales were more likely to swim slower and turn more than when cue rate was lower. During the night, fin whales were also more likely to swim slower and turn more than during the day. In addition, we examined whether the presence of singing fin whales was related to time and sea state using generalized additive models. Fin whale track presence was affected by day of the year and song season, and possibly also wind speed and wave height. Although the track kinematics from the fin whale tracks presented here are limited to a subset of whales that are acoustically active, they provide some of the only detailed movements of fin whales in the region and can be compared against fin whale swim speeds in other regions. Understanding how fin whale swimming behavior varies based on their vocalization patterns, time, and environmental factors will help us to contextualize potential changes in whale behavior during Navy training and testing on the range.

Singing strategies are linked to perch use on foraging territories in heart-nosed bats

Acoustic communication allows animals to coordinate and optimize resource utilization in space. Cardioderma cor, the heart-nosed bat, is one of the few species of bats known to sing during nighttime foraging. Previous research found that heart-nosed bats react aggressively to song playback, supporting the territorial defense hypothesis of singing in this species. By tracking 14 individuals nightly during the dry seasons in Tanzania we further investigated the territorial defense hypothesis from an ecological standpoint, which predicts singing should be associated with exclusive areas containing a resource. We quantified the singing behavior of individuals at all perches used throughout the night. Using home range analysis tools, we quantified overall use night ranges and singing ranges, as well as areas used in early and later time periods at night. Males engaged in antiphonal singing from small (x̄ = 3.48 ± 2.71 ha), largely exclusive areas that overlapped with overall night ranges used for gleaning prey. Individuals varied in singing effort; however, all sang significantly more as night progressed. Subsequently, areas used earlier at night and overall use areas were both larger than singing areas. Individuals varied in singing strategies. Some males sang for long periods in particular trees and had smaller core areas, while others moved frequently among singing trees. The most prolific singers used more perches overall. The results support the hypothesis that acoustic communication repertoires evolved in support of stable foraging territory advertisement and defense in some bats.

Humpback Whale (Megaptera novaeangliae) Song on a Subarctic Feeding Ground

Male humpback whales (Megaptera novaeangliae) are known to produce long complex sequences of structured vocalizations called song. Singing behavior has traditionally been associated with low latitude breeding grounds but is increasingly reported outside these areas. This study provides the first report of humpback whale songs in the subarctic waters of Northern Norway using a long-term bottom-moored hydrophone. Data processed included the months January–June 2018 and December 2018–January 2019. Out of 189 days with recordings, humpback whale singing was heard on 79 days. Singing was first detected beginning of January 2018 with a peak in February and was heard until mid-April. No singing activity was found during the summer months and was heard again in December 2018, continuing over January 2019. A total of 131 song sessions, including 35 full sessions, were identified throughout the study period. The longest and shortest complete sessions lasted 815 and 13 min, respectively. The results confirm that singing can be heard over several months in winter and spring on a high latitude feeding ground. This provides additional evidence to the growing literature that singing is not an explicit behavior confined to low latitude breeding grounds. The peak of song occurrence in February appears to coincide with the reproductive cycle of humpback whales. Finally, this study indicates that song occurrence on a subarctic feeding ground likely aids the cultural transmission for the North Atlantic humpback whale population.

Sex-Biased Gene Expression and Evolution in the Cerebrum and Syrinx of Chinese Hwamei (Garrulax canorus)

It is common that males and females display sexual dimorphisms, which usually result from sex-biased gene expression. Chinese hwamei (Garrulax canorus) is a good model for studying sex-biased gene expression because the song between the sexes is quite different. In this study, we analyze cerebrum and syrinx sex-biased gene expression and evolution using the de novo assembled Chinese hwamei transcriptome. In both the cerebrum and syrinx, our study revealed that most female-biased genes were actively expressed in females only, while most male-biased genes were actively expressed in both sexes. In addition, both male- and female-biased genes were enriched on the putative Z chromosome, suggesting the existence of sexually antagonistic genes and the insufficient dosage compensation of the Z-linked genes. We also identified a 9 Mb sex linkage region on the putative 4A chromosome which enriched more than 20% of female-biased genes. Resultantly, male-biased genes in both tissues had significantly higher Ka/Ks and effective number of codons (ENCs) than unbiased genes, and this suggested that male-biased genes which exhibit accelerated divergence may have resulted from positive selection. Taken together, our results initially revealed the reasons for the differences in singing behavior between males and females of Chinese hwamei.

Born to sing! Song development in a singing primate

In animal vocal communication, the development of adult-like vocalization is fundamental to interact appropriately with conspecifics. However, the factors that guide ontogenetic changes in the acoustic features remains poorly understood. In contrast with a historical view of nonhuman primate vocal production as substantially innate, recent research suggests that inheritance and physiological modification can only explain some of the developmental changes in call structure during growth. A particular case of acoustic communication is the indris' singing behavior, a peculiar case among Strepsirrhine primates. Thanks to a decade of intense data collection, this work provides the first long-term quantitative analysis on song development in a singing primate. To understand the ontogeny of such a complex vocal output, we investigated juvenile and sub-adult indris' vocal behaviour, and we found that young individuals started participating in the chorus years earlier than previously reported. Our results indicated that spectro-temporal song parameters underwent essential changes during growth. In particular, the age and sex of the emitter influenced the indris' vocal activity. We found that frequency parameters showed consistent changes across the sexes, but the temporal features showed different developmental trajectories for males and females. Given the low level of morphological sexual dimorphism and the marked differences in vocal behavior, we hypothesize that factors like social influences and auditory feedback may affect songs' features, resulting in high vocal flexibility in juvenile indris. This trait may be pivotal in a species that engages in choruses with rapid vocal turn-taking.