Sympatry drives colour and song evolution in wood-warblers (Parulidae).

Closely related species often exhibit similarities in appearance and behaviour, yet when related species exist in sympatry, signals may diverge to enhance species recognition. Prior comparative studies provided mixed support for this hypothesis, but the relationship between sympatry and signal divergence is likely nonlinear. Constraints on signal diversity may limit signal divergence, especially when large numbers of species are sympatric. We tested the effect of sympatric overlap on plumage colour and song divergence in wood-warblers (Parulidae), a speciose group with diverse visual and vocal signals. We also tested how number of sympatric species influences signal divergence. Allopatric species pairs had overall greater plumage and song divergence compared to sympatric species pairs. However, among sympatric species pairs, plumage divergence positively related to the degree of sympatric overlap in males and females, while male song bandwidth and syllable rate divergence negatively related to sympatric overlap. In addition, as the number of species in sympatry increased, average signal divergence among sympatric species decreased, which is likely due to constraints on warbler perceptual space and signal diversity. Our findings reveal that sympatry influences signal evolution in warblers, though not always as predicted, and that number of sympatric species can limit sympatry's influence on signal evolution.

Social and physiological drivers of rapid colour change in a tropical toad.

Dynamic sexual dichromatism occurs when males and females differ in colouration for a limited time. Although this trait has been primarily studied in cephalopods, chameleons, and fishes, recent analyses suggest that dynamic dichromatism is prevalent among anurans and may be mediated through sexual selection and sex recognition. Yellow toads, Incilius luetkenii, exhibit dynamic dichromatism during explosive breeding events at the onset of the rainy season: males change from a cryptic brown to a bright yellow and back again during the brief mating event. We tested the hypothesis that dynamic dichromatism in yellow toads is influenced by conspecific interactions and mediated through sex hormones and stress hormones. We placed male toads into one of four social treatments (with three other males, one male, one female, or no other toads). Immediately before and after each one-hour treatment, we quantified male colour with a reflectance spectrometer and we collected a blood sample to assess plasma concentrations of both testosterone and corticosterone. We found that males held with conspecific animals showed the brightest yellow colour and showed little or no change in their corticosterone levels. Across treatments, toads with duller yellow colour had higher levels of corticosterone. Male colour showed no association with testosterone. Interestingly, males showed substantial temporal variation in colour and corticosterone: toads were duller yellow and exhibited greater levels of corticosterone post-treatment across subsequent days at the onset of the rainy season. Our findings reveal that both conspecific interactions and corticosterone are involved in the dynamic colour change of yellow toads.

Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning.

Vocal learning, in which animals modify their vocalizations based on social experience, has evolved in several lineages of mammals and birds, including humans. Despite much attention, the question of how this key cognitive trait has evolved remains unanswered. The motor theory for the origin of vocal learning posits that neural centres specialized for vocal learning arose from adjacent areas in the brain devoted to general motor learning. One prediction of this hypothesis is that visual displays that rely on complex motor patterns may also be learned in taxa with vocal learning. While learning of both spoken and gestural languages is well documented in humans, the occurrence of learned visual displays has rarely been examined in non-human animals. We tested for geographical variation consistent with learning of visual displays in long-billed hermits ( Phaethornis longirostris), a lek-mating hummingbird that, like humans, has both learned vocalizations and elaborate visual displays. We found lek-level signatures in both vocal parameters and visual display features, including display element proportions, sequence syntax and fine-scale parameters of elements. This variation was not associated with genetic differentiation between leks. In the absence of genetic differences, geographical variation in vocal signals at small scales is most parsimoniously attributed to learning, suggesting a significant role of social learning in visual display ontogeny. The co-occurrence of learning in vocal and visual displays would be consistent with a parallel evolution of these two signal modalities in this species.

Hot temperatures during the dry season reduce survival of a resident tropical bird.

Understanding how climate change will shape species distributions in the future requires a functional understanding of the demographic responses of animals to their environment. For birds, most of our knowledge of how climate influences population vital rates stems from research in temperate environments, even though most of Earth's avian diversity is concentrated in the tropics. We evaluated effects of Southern Oscillation Index (SOI) and local temperature and rainfall at multiple temporal scales on sex-specific survival of a resident tropical bird, the rufous-and-white wren Thryophilus rufalbus, studied over 15 years in the dry forests of northwestern Costa Rica. We found that annual apparent survival of males was 8% higher than females, more variable over time, and responded more strongly to environmental variation than female survival, which did not vary strongly with SOI or local weather. For males, mean and maximum local temperatures were better predictors of survival than either rainfall or SOI, with high temperatures during the dry season and early wet season negatively influencing survival. These results suggest that, even for species adapted to hot environments, further temperature increases may threaten the persistence of local populations in the absence of distributional shifts.

Parallel evolutionary forces influence the evolution of male and female songs in a tropical songbird.

Given the important role that animal vocalizations play in mate attraction and resource defence, acoustic signals are expected to play a significant role in speciation. Most studies, however, have focused on the acoustic traits of male animals living in the temperate zone. In contrast to temperate environments, in the tropics, it is commonplace for both sexes to produce complex acoustic signals. Therefore, tropical birds offer the opportunity to compare the sexes and provide a more comprehensive understanding of the evolution of animal signals. In this study, we quantified patterns of acoustic variation in Rufous-and-white Wrens (Thryophilus rufalbus) from five populations in Central America. We quantified similarities and differences between male and female songs by comparing the role that acoustic adaptation, cultural isolation and neutral genetic divergence have played in shaping acoustic divergence. We found that males and females showed considerable acoustic variation across populations, although females exhibited greater population divergence than males. Redundancy analysis and partial-redundancy analysis revealed significant relationships between acoustic variation and ecological variables, genetic distance, and geographic distance. Both ambient background noise and geographic distance explained a high proportion of variance for both males and females, suggesting that both acoustic adaptation and cultural isolation influence song. Overall, our results indicate that parallel evolutionary forces act on male and female acoustic signals and highlight the important role that cultural drift and selection play in the evolution of both male and female songs.

The biogeographic and evolutionary history of an endemic clade of Middle American sparrows: Melozone and Aimophila (Aves: Passerellidae).

The large number of endemic species in Middle America is frequently attributed to the interplay of geographical barriers and historical climatic changes in the region. This process promotes genetic divergence between populations, and given enough time, may yield new species. Animals that inhabit mid-elevation or highland habitats may be disproportionately affected in this way. Genetic analyses of animals in this region allow us to better understand how historical patterns of isolation have influenced the generation of new species in this biodiversity hotspot. We studied the biogeography and systematics of two closely related genera of sparrows (Passerellidae): Melozone and Aimophila. Collectively, this group is distributed from the southwestern United States and southward as far as central Costa Rica. We sampled 81 individuals of 8 Melozone and 2 Aimophila species, from 19 localities distributed throughout their ranges. We reconstructed phylogenetic relationships and time-calibrated species trees using multilocus sequence data comprised of one mitochondrial gene and five nuclear genes. We conducted an ancestral area reconstruction analysis to determine the probability of ancestral range at each divergent event. Despite analyzing six loci, we were unable to obtain a fully resolved phylogenetic tree. We recovered four main lineages: lineage 1 includes four Melozone species distributed north of Isthmus of Tehuantepec (M. albicollis, M. crissalis, M. aberti, M. fusca); lineage 2 includes three Melozone species distributed south of the Isthmus of Tehuantepec (M. biarcuata, M. cabanisi, M. leucotis); lineage 3 lineage consists of a single species endemic to the Pacific coast of Mexico (M. kieneri); and lineage 4 includes the more widely distributed sparrows in the genus Aimophila. Our analyses suggest that these genera probably originated during the late Miocene in the Madrean Highlands of southern Mexico. We identified dispersal as the prevalent cause of speciation in this clade with most lineages dispersing to their current distributions from southern Mexico either to the north following a developing and expanding Madro-Tertiary flora, or to the south across the Isthmus of Tehuantepec. A similar pattern of dispersal from this biogeographic region has been reported in other taxa including fishes, reptiles, and birds. Our results reveal that the four lineages identified represent geographically coherent and ecologically similar assemblages of taxa. Finally, when our genetic results are considered, along with apparent differences in morphology and song, the allopatric forms M. b. cabanisi and M. l. occipitalis warrant recognition as biological species.

Male song sparrows have elevated testosterone in response to neighbors versus strangers.

Upon hearing a conspecific signal, animals must assess their relationship with the signaller and respond appropriately. Territorial animals usually respond more aggressively to strangers than neighbors in a phenomenon known as the "dear enemy effect". This phenomenon likely evolved because strangers represent a threat to an animal's territory tenure and parentage, whereas neighbors only represent a threat to an animal's parentage because they already possess a territory (providing territory boundaries are established and stable). Although the dear enemy effect has been widely documented using behavioral response variables, little research has been conducted on the physiological responses of animals to neighbors versus strangers. We sought to investigate whether the dear enemy effect is observed physiologically by exposing territorial male song sparrows (Melospiza melodia) to playback simulating a neighbor or a stranger, and then collecting blood samples to measure plasma testosterone levels. We predicted that song sparrows would exhibit increased testosterone levels after exposure to stranger playback compared to neighbor playback, due to the role testosterone plays in regulating aggression. Contrary to our prediction, we found that song sparrows had higher testosterone levels after exposure to neighbor playback compared to stranger playback. We discuss several explanations for our result, notably that corticosterone may regulate the dear enemy effect in male song sparrows and this may inhibit plasma testosterone. Future studies will benefit from examining corticosterone in addition to testosterone, to better understand the hormonal underpinnings of the dear enemy effect.

Operant discrimination of relative frequency ratios in black-capped chickadee song.

The two-note fee bee song of the black-capped chickadee (Poecile atricapillus) is sung at many different absolute frequencies, but the relative frequencies, or "pitch ratios", between the start and end of the fee note (glissando) and the fee and the bee notes (inter-note interval) are preserved with each pitch-shift. Ability to perceive these ratios and their relative salience varies with sex of the bird and setting: while both sexes appear to perceive changes in the inter-note interval, males appear to attend to the glissando in the field, and females appear to attend to both ratios. In this study, we compared directly whether male and female chickadees could discriminate between normal fee bee songs and songs that had one or both of the pitch ratios altered, and whether birds attended to one type of alteration over another. Both sexes learned to discriminate normal from altered songs; songs lacking an inter-note interval were more easily discriminated than songs with only the glissando removed. Females performed slightly better than males, including in the most difficult task with the stimuli lacking the glissando. Our study illustrates the value of using perceptual tasks to directly compare performance between the sexes and to demonstrate the difference between perception of and attention to acoustic features of vocal communication.

Playback responses of socially monogamous black-fronted titi monkeys to simulated solitary and paired intruders.

Many birds and primates use loud vocalizations to mediate agonistic interactions with conspecifics, either as solos by males or females, or as coordinated duets. The extensive variation in duet complexity, the contribution of each sex, and the context in which duets are produced suggest that duets may serve several functions, including territory and mate defense. Titi monkeys (Callicebus spp.) are believed to defend their home range via solo loud calls or coordinated duets. Yet there are remarkably few experimental studies assessing the function of these calls. Observations of interactions between wild established groups and solitary individuals are rare and, therefore, controlled experiments are required to simulate such situations and evaluate the mate and joint territorial defense hypotheses. We conducted playback experiments with three free-ranging groups of habituated black-fronted titi monkeys (Callicebus nigrifrons) to test these hypotheses. We found that titi monkeys responded to the three conspecific playback treatments (duets, female solos, and male solos) and did not respond to the heterospecific control treatment. The monkeys did not show sex-specific responses to solos (N = 12 trials). Partners started to duet together in 79% of their responses to playback-simulated rivals (N = 14 calls in response to playback). Males started to approach the loudspeaker before females regardless of the type of stimulus. The strength of the response of mated pairs to all three conspecific treatments was similar. Overall, our results are consistent with the idea that black-fronted titi monkeys use their loud calls in intergroup communication as a mechanism of joint territorial defense.

Uneven sampling and the analysis of vocal performance constraints.

Studies of trilled vocalizations provide a premiere illustration of how performance constraints shape the evolution of mating displays. In trill production, vocal tract mechanics impose a trade-off between syllable repetition rate and frequency bandwidth, with the trade-off most pronounced at higher values of both parameters. Available evidence suggests that trills that simultaneously maximize both traits are more threatening to males or more attractive to females, consistent with a history of sexual selection favoring high-performance trills. Here, we identify a sampling limitation that confounds the detection and description of performance trade-offs. We reassess 70 data sets (from 26 published studies) and show that sampling limitations afflict 63 of these to some degree. Traditional upper-bound regression, which does not control for sampling limitations, detects performance trade-offs in 33 data sets; yet when sampling limitations are controlled, performance trade-offs are detected in only 15. Sampling limitations therefore confound more than half of all performance trade-offs reported using the traditional method. An alternative method that circumvents this sampling limitation, which we explore here, is quantile regression. Our goal is not to question the presence of mechanical trade-offs on trill production but rather to reconsider how these trade-offs can be detected and characterized from acoustic data.

Vocal behavior of black-fronted titi monkeys (Callicebus nigrifrons): acoustic properties and behavioral contexts of loud calls.

Loud calls can be heard over long distances due to their high amplitude and low frequency. These calls are commonly used for both within- and between-group communication in many bird and primate species. In the Neotropics, mated pairs of socially monogamous titi monkeys (genus Callicebus) emit conspicuous, coordinated loud calls. These vocalizations appear to play a role in territorial defense, a hypothesis derived from studies of only three of the 31 recognized Callicebus species. Here, we describe the acoustic properties and organization of the loud calls of black-fronted titi monkeys (Callicebus nigrifrons). We compare the behavioral and ecological contexts associated with these vocalizations to investigate their role in within- and between-group communication, resource defense, and mate defense. Black-fronted titi monkeys create loud calls by combining a finite number of syllables to form more complex phrases, which are assembled to compose long sequences of loud calls. Bioacoustic features distinguish the loud calls used in different contexts, involving communication within- and between-groups. We found support for the hypothesis that vocalizations used for between-group communication are cooperative displays used by the mated pair and other group members to regulate access to important food resources, such as fruits. On the other hand, we only found weak support for the mate defense hypothesis.

Acoustic similarity of flight calls corresponds with the composition and structure of mixed-species flocks of migrating birds: evidence from a three-dimensional microphone array.

Animals that migrate in mixed-species groups may communicate with both conspecific and heterospecific individuals, providing a low-cost mechanism for navigation whenever individuals share similar migratory routes or destinations. Many migratory birds produce calls while flying, but the function of these calls, and the forces contributing to their evolution, are poorly known. We studied flight calls in mixed-species groups of wood warblers (Parulidae), a biodiverse group of migratory songbirds. We used a spatial approach to examine whether acoustic similarity of flight calls varies with group composition, recording flight calls of mixed-species flocks with a wireless microphone array and triangulating the positions of birds in three dimensions. We found that the acoustic similarity of flight calls was correlated with spatial proximity: birds with similar calls fly closer together during migration. We also found relationships between acoustic similarity, flock size and mixed-species flock diversity: birds with similar calls fly in smaller flocks and in flocks with lower species diversity. Our results support the idea that migrating birds use flight calls to maintain contact with acoustically similar individuals in mixed-species flocks, with communication transcending species boundaries. These results suggest that acoustically similar flight calls are used as cues of group assembly for migratory animals. This article is part of the theme issue 'Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes'.

Cumulative cultural evolution and mechanisms for cultural selection in wild bird songs.

Cumulative cultural evolution, the accumulation of sequential changes within a single socially learned behaviour that results in improved function, is prominent in humans and has been documented in experimental studies of captive animals and managed wild populations. Here, we provide evidence that cumulative cultural evolution has occurred in the learned songs of Savannah sparrows. In a first step, "click trains" replaced "high note clusters" over a period of three decades. We use mathematical modelling to show that this replacement is consistent with the action of selection, rather than drift or frequency-dependent bias. Generations later, young birds elaborated the "click train" song form by adding more clicks. We show that the new songs with more clicks elicit stronger behavioural responses from both males and females. Therefore, we suggest that a combination of social learning, innovation, and sexual selection favoring a specific discrete trait was followed by directional sexual selection that resulted in naturally occurring cumulative cultural evolution in the songs of this wild animal population.

Natal experience and pre-breeding environmental conditions affect lay date plasticity in Savannah Sparrows.

Phenotypic plasticity allows organisms to adjust the timing of life-history events in response to environmental and demographic conditions. Shifts by individuals in the timing of breeding with respect to variation in age and temperature are well documented in nature, and these changes are known to scale to affect population dynamics. However, relatively little is known about how organisms alter phenology in response to other demographic and environmental factors. We investigated how pre-breeding temperature, breeding population density, age, and rainfall in the first month of life influenced the timing and plasticity of lay date in a population of Savannah Sparrows (Passerculus sandwichensis) monitored over 33 yr (1987-2019). Females that experienced warmer pre-breeding temperatures tended to lay eggs earlier, as did older females, but breeding population density had no effect on lay date. Natal precipitation interacted with age to influence lay date plasticity, with females that experienced high precipitation levels as nestlings advancing lay dates more strongly over the course of their lives. We also found evidence for varied pace of life; females that experienced high natal precipitation had shorter lifespans and reduced fecundity, but more nesting attempts over their lifetimes. Rainfall during the nestling period increased through time, while population density and fecundity declined, suggesting that increased precipitation on the breeding grounds may be detrimental to breeding females and ultimately the viability of the population as a whole. Our results suggest that females adjust their laying date in response to pre-breeding temperature, and as they age, while presenting new evidence that environmental conditions during the natal period can affect phenological plasticity and generate downstream, population-level effects.

Context-dependent functions of avian duets revealed by microphone-array recordings and multispeaker playback.

In many tropical animals, male and female breeding partners combine their songs to produce vocal duets [1-5]. Duets are often so highly coordinated that human listeners mistake them for the songs of a single animal [6]. Behavioral ecologists rank duets among the most complex vocal performances in the animal kingdom [7, 8]. Despite much research, the evolutionary significance of duets remains elusive [9], in part because many duetting animals live in tropical habitats where dense vegetation makes behavioral observation difficult or impossible. Here, we evaluate the duetting behavior of rufous-and-white wrens (Thryothorus rufalbus) in the humid forests of Costa Rica. We employ two innovative technical approaches to study duetting behavior: an eight-microphone acoustic location system capable of triangulating animals' positions on the basis of recordings of their vocalizations [10] and dual-speaker playback capable of simulating duets in a spatially realistic manner [11]. Our analyses provide the first detailed spatial information on duetting in both a natural context and during confrontations with rivals. We demonstrate that birds perform duets across highly variable distances, that birds approach their partner after performing duets, and that duets of rivals induce aggressive, sex-specific responses. We conclude that duets serve distinct functions in aggressive and nonaggressive contexts.

Anthropogenic noise affects song structure in red-winged blackbirds (Agelaius phoeniceus).

Anthropogenic noise can mask animal signals that are crucial for communicating information about food, predators and mating opportunities. In response to noise masking, signallers can potentially improve acoustic signal transmission by adjusting the timing, frequency or amplitude of their signals. These changes can be a short-term modification in response to transient noise or a long-term modification in response to chronic noise. An animal's ability to adapt to anthropogenic noise can be crucial to its success. In this study, we evaluated the effects of anthropogenic noise on the structure of red-winged blackbird song. First, we manipulated the presence of anthropogenic noise by experimentally broadcasting either silence or low-frequency white noise to subjects inhabiting quiet marshes located away from roadsides. Subjects exhibited increased signal tonality when temporarily exposed to low-frequency white noise, suggesting that red-winged blackbirds can alter their signals rapidly in response to sudden noise. Second, we compared songs produced in quiet marshes located away from roadsides with songs produced during quiet periods at roadside marshes that are normally noisy. This allowed us to test whether birds that are exposed to chronic anthropogenic noise exhibit altered song structure during temporarily quiet periods. Subjects residing in roadside marshes that are normally polluted with anthropogenic noise sang songs with increased tonality during quiet periods. Overall, our results show that anthropogenic noise influences the structure of birdsong. These effects should be considered in conservation and wildlife management.

The evolution of wood warbler flight calls: Species with similar migrations produce acoustically similar calls.

Diverse animal species engage in long-distance migrations. Many migrants travel in groups, and communication within these groups may be important to survival and successful migration. We examined migration and communication in 36 species of wood warblers (Parulidae), songbirds that breed in North America and migrate in mixed-species flocks to their wintering grounds. During migration, wood warblers produce short vocalizations called "flight calls." The function of flight calls and the patterns of acoustic similarity between species are poorly understood. We investigated whether acoustic similarity of flight calls of different species of warbler reflects the similarity in their migratory journeys or their phylogenetic relatedness. We found that phylogeny, similarity in breeding latitude, and overlap in the timing of migration predict acoustic flight call similarity across warbler species. Further, we found that phylogeny, similarity in migration distance, and overlap in wintering range predict acoustic flight call similarity in a subset of 12 species with highly similar calls, although this analysis has a small sample size. We conclude that migratory similarity may be an important force driving the evolution of acoustically similar calls in wood warblers, in addition to phylogenetic relatedness. Acoustic convergence in these species may facilitate communication between individuals with similar migrations.

Dynamic sexual dichromatism in an explosively breeding Neotropical toad.

Sexual selection often promotes the evolution of elaborate colour signals in males, but the importance of sexually selected colour signals remains poorly studied in amphibians. We used reflectance spectrometry to document pronounced sexual dichromatism and dramatic colour change in Bufo luetkenii, a toad that breeds in large aggregations at the onset of the rainy season in Costa Rica. Our observations suggest that males fade rapidly from a vibrant lemon yellow to a dull brown once they have paired with a female. We demonstrate this by showing that males are much brighter than females and that unpaired males are more colourful than males in amplexus. We also show that coloration fades rapidly when males are briefly held captive. This is, to our knowledge, the first study to document such dynamic change in male coloration and sexual dichromatism in anurans.

Wild Birds Learn Songs from Experimental Vocal Tutors.

In eight groups of animals, including humans and songbirds, juveniles are understood to learn vocalizations by listening to adults [1-4]. Experimental studies of laboratory-reared animals support this hypothesis for vocal learning [5-7], yet we lack experimental evidence of vocal learning in wild animals. We developed an innovative playback technology involving automated loudspeakers that broadcast songs with distinctive acoustic signatures. We used this technology to simulate vocal tutors in the wild and conducted year-long tutoring sessions to five cohorts of free-living migratory Savannah Sparrows in eastern Canada. We confirm that wild birds learn songs by listening to adult conspecific animals, and we show that they pass these songs on to subsequent generations. Further, we provide the first experimental evidence in the wild that the timing of exposure to tutor song influences vocal learning: wild Savannah Sparrows preferentially learn songs heard during both their natal summer and at the outset of their first breeding season. This research provides direct experimental evidence of song learning by wild animals and shows that wild birds learn songs during two critical stages of development early in life. VIDEO ABSTRACT.

The Evolution of Signal Design in Manakin Plumage Ornaments.

Animal signals are characterized by two design components: efficacy (detectability) and content (message being conveyed). Selection for efficient signal perception should favor the evolution of traits that exhibit an optimal balance between these two design components. We examined the evolution of signal design in the colorful plumage ornaments of manakins (Aves: Pipridae). We used a model of avian color space to quantify how differences in plumage coloration would be perceived by a typical passerine bird and examined patterns of coloration across 50 species of manakin. Using phylogenetically independent contrasts, we show that plumage contrast against the background increases with sexual dichromatism in males but not females, suggesting that sexual selection has favored the evolution of male plumage ornaments that enhance signal efficacy. Plumage contrast within individuals also increased with dichromatism in males but not females. Finally, plumage colors produced by different mechanisms, which may reveal different aspects of quality, resulted in different degrees of contrast against the background. Our findings suggest that selection for signal efficacy and content may sometimes be opposing, creating a trade-off between these two components of signal design. Manakins may mediate this trade-off by combining multiple plumage ornaments that differ in efficacy and content.