A machine learning approach for classifying and quantifying acoustic diversity.

1. Assessing diversity of discretely varying behavior is a classical ethological problem. In particular, the challenge of calculating an individuals' or species' vocal repertoire size is often an important step in ecological and behavioral studies, but a reproducible and broadly applicable method for accomplishing this task is not currently available. 2. We offer a generalizable method to automate the calculation and quantification of acoustic diversity using an unsupervised random forest framework. We tested our method using natural and synthetic datasets of known repertoire sizes that exhibit standardized variation in common acoustic features as well as in recording quality. We tested two approaches to estimate acoustic diversity using the output from unsupervised random forest analyses: (i) cluster analysis to estimate the number of discrete acoustic signals (e.g., repertoire size) and (ii) an estimation of acoustic area in acoustic feature space, as a proxy for repertoire size. 3. We find that our unsupervised analyses classify acoustic structure with high accuracy. Specifically, both approaches accurately estimate element diversity when repertoire size is small to intermediate (5-20 unique elements). However, for larger datasets (20-100 unique elements), we find that calculating the size of the area occupied in acoustic space is a more reliable proxy for estimating repertoire size. 4. We conclude that our implementation of unsupervised random forest analysis offers a generalizable tool that researchers can apply to classify acoustic structure of diverse datasets. Additionally, output from these analyses can be used to compare the distribution and diversity of signals in acoustic space, creating opportunities to quantify and compare the amount of acoustic variation among individuals, populations, or species in a standardized way. We provide R code and examples to aid researchers interested in using these techniques.

Correlated evolution of distinct signals associated with increased social selection in female white-shouldered fairywrens.

Conspicuous female signals have recently received substantial scientific attention, but it remains unclear if their evolution is the result of selection acting on females independently of males or if mutual selection facilitates female change. Species that express female, but not male, phenotypic variation among populations represents a useful opportunity to address this knowledge gap. White-shouldered fairywrens (Malurus alboscapulatus) are tropical songbirds with a well-resolved phylogeny where female, but not male, coloration varies allopatrically across subspecies. We explored how four distinct signaling modalities, each putatively associated with increased social selection, are expressed in two populations that vary in competitive pressure on females. Females in a derived subspecies (M. a. moretoni) have evolved more ornamented plumage and have shorter tails (a signal of social dominance) relative to an ancestral subspecies (M. a. lorentzi) with drab females. In response to simulated territorial intrusions broadcasting female song, both sexes of M. a. moretoni are more aggressive and more coordinated with their mates in both movement and vocalizations. Finally, M. a. moretoni songs are more complex than M. a. lorentzi, but song complexity does not vary between sexes in either population. These results suggest that correlated phenotypic shifts in coloration and tail morphology in females as well as song complexity and aggression in both sexes may have occurred in response to changes in the intensity of social selection pressures. This highlights increased competitive pressures in both sexes can facilitate the evolution of complex multimodal signals.

Comparative bioacoustics: a roadmap for quantifying and comparing animal sounds across diverse taxa.

Animals produce a wide array of sounds with highly variable acoustic structures. It is possible to understand the causes and consequences of this variation across taxa with phylogenetic comparative analyses. Acoustic and evolutionary analyses are rapidly increasing in sophistication such that choosing appropriate acoustic and evolutionary approaches is increasingly difficult. However, the correct choice of analysis can have profound effects on output and evolutionary inferences. Here, we identify and address some of the challenges for this growing field by providing a roadmap for quantifying and comparing sound in a phylogenetic context for researchers with a broad range of scientific backgrounds. Sound, as a continuous, multidimensional trait can be particularly challenging to measure because it can be hard to identify variables that can be compared across taxa and it is also no small feat to process and analyse the resulting high-dimensional acoustic data using approaches that are appropriate for subsequent evolutionary analysis. Additionally, terminological inconsistencies and the role of learning in the development of acoustic traits need to be considered. Phylogenetic comparative analyses also have their own sets of caveats to consider. We provide a set of recommendations for delimiting acoustic signals into discrete, comparable acoustic units. We also present a three-stage workflow for extracting relevant acoustic data, including options for multivariate analyses and dimensionality reduction that is compatible with phylogenetic comparative analysis. We then summarize available phylogenetic comparative approaches and how they have been used in comparative bioacoustics, and address the limitations of comparative analyses with behavioural data. Lastly, we recommend how to apply these methods to acoustic data across a range of study systems. In this way, we provide an integrated framework to aid in quantitative analysis of cross-taxa variation in animal sounds for comparative phylogenetic analysis. In addition, we advocate the standardization of acoustic terminology across disciplines and taxa, adoption of automated methods for acoustic feature extraction, and establishment of strong data archival practices for acoustic recordings and data analyses. Combining such practices with our proposed workflow will greatly advance the reproducibility, biological interpretation, and longevity of comparative bioacoustic studies.

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy-wrens.

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male-female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year-round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine-fairy-wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life-history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male-female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.

Breeding season length predicts duet coordination and consistency in Neotropical wrens (Troglodytidae).

Many animals produce coordinated signals, but few are more striking than the elaborate male-female vocal duets produced by some tropical songbirds. Yet, little is known about the factors driving the extreme levels of vocal coordination between mated pairs in these taxa. We examined evolutionary patterns of duet coordination and their potential evolutionary drivers in Neotropical wrens (Troglodytidae), a songbird family well known for highly coordinated duets. Across 23 wren species, we show that the degree of coordination and precision with which pairs combine their songs into duets varies by species. This includes some species that alternate their song phrases with exceptional coordination to produce rapidly alternating duets that are highly consistent across renditions. These highly coordinated, consistent duets evolved independently in multiple wren species. Duet coordination and consistency are greatest in species with especially long breeding seasons, but neither duet coordination nor consistency are correlated with clutch size, conspecific abundance or vegetation density. These results suggest that tightly coordinated duets play an important role in mediating breeding behaviour, possibly by signalling commitment or coalition of the pair to mates and other conspecifics.

New insights from female bird song: towards an integrated approach to studying male and female communication roles.

Historically, bird song has been regarded as a sex-specific signalling trait; males sing to attract females and females drive the evolution of signal exaggeration by preferring males with ever more complex songs. This view provides no functional role for female song. Historic geographical research biases generalized pronounced sex differences of phylogenetically derived northern temperate zone songbirds to all songbirds. However, we now know that female song is common and that both sexes probably sang in the ancestor of modern songbirds. This calls for research on adaptive explanations and mechanisms regulating female song, and a reassessment of questions and approaches to identify selection pressures driving song elaboration in both sexes and subsequent loss of female song in some clades. In this short review and perspective we highlight newly emerging questions and propose a research framework to investigate female song and song sex differences across species. We encourage experimental tests of mechanism, ontogeny, and function integrated with comparative evolutionary analyses. Moreover, we discuss the wider implications of female bird song research for our understanding of male and female communication roles.

Differentiating the evolution of female song and male-female duets in the New World blackbirds: can tropical natural history traits explain duet evolution?

Female bird song and combined vocal duets of mated pairs are both frequently associated with tropical, monogamous, sedentary natural histories. Little is known, however, about what selects for duetting behavior versus female song. Female song likely preceded duet evolution and could drive apparent relationships between duets and these natural histories. We compared the evolution of female song and male-female duets in the New World blackbirds (Icteridae) by investigating patterns of gains and losses of both traits and their relationships with breeding latitude, mating system, nesting pattern, and migratory behavior. We found that duets evolved only in lineages in which female song was likely ancestral. Both female song and duets were correlated with tropical breeding, social monogamy, territorial nesting, and sedentary behavior when all taxa were included; however, correlations between duets and these natural history traits disappeared when comparisons were limited to taxa with female song. Also, likelihood values supported stronger relationships between the natural history traits and female song than between these traits and duets. Our results suggest that the natural histories thought to favor the evolution of duetting may in fact be associated with female song and that additional selection pressures are responsible for the evolution of duets.

Female song is widespread and ancestral in songbirds.

Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwin's theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes.