CORRELATED EVOLUTION OF BEAK MORPHOLOGY AND SONG IN THE NEOTROPICAL WOODCREEPER RADIATION

Mating signals may diversify as a byproduct of morphological adaptation to different foraging niches, potentially driving speciation. Although many studies have focused on the direct influence of ecological and sexual selection on signal divergence, the role of indirect mechanisms remains poorly understood. Using phenotypic and molecular datasets, we explored the interplay between morphological and vocal evolution in an avian radiation characterized by dramatic beak variation, the Neotropical woodcreepers (Dendrocolaptinae). We found evidence of a trade-off between the rate of repetition of song syllables and frequency bandwidth: slow paced songs had either narrow or wide frequency bandwidths, and bandwidth decreased as song pace increased. This bounded phenotypic space for song structure supports the hypothesis that passerine birds face a motor constraint during song production. Diversification of acoustic characters within this bounded space was correlated with diversification of beak morphology. In particular, species with larger beaks produced slower songs with narrower frequency bandwidths, suggesting that ecological selection on beak morphology influences the diversification of woodcreeper songs. Because songs in turn mediate mate choice and species recognition in birds, these results indicate a broader role for ecology in avian diversification.     

Differentiation of Mating Vocalizations in Birds: Acoustic Features in Mainland and Island Populations and Evidence of Habitat-Dependent Selection on Songs

Local environments can act as selective agents on some characteristics of birds’ songs, whereas other song traits may not reflect local genetic adaptation. Geographic variation in songs of two Australian bird species (red‐capped robins Petroica goodenovii, western gerygones Gerygone fusca) was studied to examine one component of the ‘habitat‐dependent selection’ hypothesis. This hypothesis suggests that: (1) the detailed spectral characteristics of male songs are an evolved response to local habitat conditions affecting signal propagation and detection and (2) parallel evolution of other fitness traits sets up the potential for assortative mating by female choice. To examine the first part of the hypothesis, I made comparisons among widespread mainland populations and an island population using two levels of analysis: a typological analysis of song morphology (phonology: notes, syllables, syntax, temporal pattern, repertoires) and a spectral analysis of acoustic characteristics of songs (mean frequency, Wiener entropy, frequency modulation) using an automated procedure of feature extraction (Sound Analysis Pro). Spectral analysis was also used to extract values of the same acoustic features from the background sound environment of each recorded population. The typological analysis revealed no differences among mainland populations of either species, but large differences between mainland songs and those on the island. In contrast, the spectral analysis revealed acoustic divergence among populations, both mainland and island. For both species, Wiener entropy of songs correlated negatively with that of the ambient sound environment, consistent with predictions of the habitat‐dependent selection hypothesis of environmental selection on signal design.     

The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation in vertebrates.     

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution. Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between‐site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic‐acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species‐specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song.     

Ecological gradient of sexual selection: elevation and song elaboration in finches

Ecological gradients in natural and sexual selection often result in evolutionary diversification of morphological, life history, and behavioral traits. In particular, elevational changes in habitat structure and climate not only covary with intensity of sexual selection in many taxa, but may also influence evolution of mating signals. Here we examined variation in courtship song in relation to elevation of breeding across cardueline finches-a subfamily of birds that occupies the widest elevational range of extant birds and shows extensive variation in life histories and sexual selection along this range. We predicted that decrease in sexual selection intensity with elevation of breeding documented in this clade would result in a corresponding evolutionary reduction in elaboration of courtship songs. We controlled for the effects of phylogeny, morphology, and habitat structure to uncover a predicted elevational decline in courtship song elaboration; species breeding at lower elevations sang more elaborated and louder songs compared to their sister species breeding at higher elevations. In addition, lower elevation species had longer songs with more notes, whereas frequency components of song did not vary with elevation. We suggest that changes in sexual selection account for the observed patterns of song variation and discuss how elevational gradient in sexual selection may facilitate divergence in mating signals potentially reinforcing or promoting speciation.     

Morphological adaptation influences the evolution of a mating signal

Theory predicts that forces of natural selection can reduce the intensity of sexually selected traits. In this study, I investigate how morphological adaptation to feeding ecology influences a mating signal. In birds, changes in feeding ecology can cause rapid divergence in bill morphology. Because bills are also important for song production, feeding ecology may influence song divergence. During song, birds can rapidly change vocal tract resonance using bill movement, yet are constrained in rate and magnitude of bill movements resulting in a trade-off between trill rate and frequency bandwidth. Male swamp sparrows vary in their ability to produce rapid, broad-band trills and females prefer more physically demanding songs. Populations of swamp sparrows adapted to the feeding ecology of tidal marshes have larger bills than inland populations. Larger bills should increase the constraints of producing rapid, broad-band trills allowing for a test of how changes in feeding ecology affect a feature of song used in mate choice. I found significant differences in acoustic features of song consistent with the hypothesis that coastal males are less able to meet the physical demands of song production because of the constraints of having larger bills. As possible compensation for decreases in song performance, coastal populations exhibit an increase in song complexity. These changes support the current model of how motor constraints influence song production and suggest a mechanism by which feeding ecology can influence signal evolution.     

Beak morphology and song features covary in a population of Darwin's finches (Geospiza fortis)

Animal mating signals evolve in part through indirect natural selection on anatomical traits that influence signal expression. In songbirds, for example, natural selection on beak form and function can influence the evolution of song features, because of the role of the beak in song production. In this study we characterize the relationship between beak morphology and song features within a bimodal population of Geospiza fortis on Santa Cruz Island, Galápagos. This is the only extant population of Darwin's finches that is known to possess a bimodal distribution in beak size. We test the hypothesis that birds with larger beaks are constrained to produce songs with lower frequencies and decreased vocal performance. We find that birds with longer, deeper, and wider beaks produce songs with significantly lower minimum frequencies, maximum frequencies and frequency bandwidths. Results from the analysis of the relationship between beak morphology and trill rate are mixed. Measures of beak morphology correlated positively with 'vocal deviation', a composite index of vocal performance. Overall these results support a resonance model of vocal tract function, and suggest that beak morphology, a primary target of ecological selection in Darwin's finches, affects the evolution of mating signals. We suggest that differences in song between the two modes of the distribution may influence mate recognition and perhaps facilitate assortative mating by beak size and population divergence.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 489–498.     

Song parameters of the fuscous honeyeater Lichenostomus fuscus correlate with habitat characteristics in fragmented landscapes

Both avian abundance and species richness decline in response to habitat loss and fragmentation. Studying variation in bird song structure across modified landscapes can provide insights into the effects of habitat alterations on coherence of social interactions within populations. Here, we tested whether fragmentation or change of habitat quality within box‐ironbark forest of central Victoria impacted cultural connectivity and song characteristics in fuscous honeyeater, a declining common Australian bird. First, we tested whether geographic distance and/or spatially‐explicit landscape connectivity models can explain patterns of song similarity across fragmented landscapes. We found no evidence that distance or habitat fragmentation impacts the nature and transmission of fuscous honeyeater song, and concluded that acoustic connectivity at the scale of our study is high. Second, we tested whether variation in habitat quality explains variation in song characteristics. In accordance with acoustic adaptation to habitat structure, birds sang longer songs in sites with more large trees and produced longer common song elements in sites with greater tree height. However, the acoustic adaptation hypothesis cannot explain the finding that in less‐disturbed landscapes with higher tree‐cover birds sang songs (and song elements) with higher maximum frequency and wider frequency bandwidth. We also found that birds sing longer and more variable songs of wider frequency bandwidth in less disturbed sites with a greater number of large mature trees, which may represent better feeding resources. Our study suggests that changes in song structure with habitat degradation could signal disturbed population processess, such as changes in the acoustic communication among resident birds.     

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission (“sensory drive”) or because morphological adaptation to different foraging niches causes divergence in “magic traits” associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.     

Songbirds learn songs least degraded by environmental transmission

Communication depends on accurate reception of signals by receivers, and selection acts on signals to transmit efficiently through the environment. Although learnt signals, such as birdsong, vary in their transmission properties through different habitats, few studies have addressed the role of cultural selection in driving acoustic adaptation. Here, we present a test of the hypothesis that song-learning birds choose to copy songs that are less degraded by transmission through the environment, using swamp sparrows (Melospiza georgiana) as our study species. We found that all subjects discriminated between undegraded and naturally degraded song models, and learnt only from undegraded song models, demonstrating a role for cultural selection in acoustic adaptation of learnt signals.     

SONG DIVERGENCE BY SENSORY DRIVE IN AMAZONIAN BIRDS

Visual signals are shaped by variation in the signaling environment through a process termed sensory drive, sometimes leading to speciation. However, the evidence for sensory drive in acoustic signals is restricted to comparisons between highly dissimilar habitats, or single‐species studies in which it is difficult to rule out the influence of undetected ecological variables, pleiotropic effects, or chance. Here we assess whether this form of sensory drive—often termed “acoustic adaptation”—can generate signal divergence across ecological gradients. By studying avian communities in two Amazonian forest types, we show that songs of 17 “bamboo‐specialist” bird species differ in predictable ways from their nearest relatives in adjacent terra firme forest. We also demonstrate that the direction of song divergence is correlated with the sound transmission properties of habitats, rather than with genetic divergence, ambient noise, or pleiotropic effects of mass and bill size. Our findings indicate that acoustic adaptation adds significantly to stochastic processes underlying song divergence, even when comparing between habitats with relatively similar structure. Furthermore, given that song differences potentially contribute to reproductive isolation, these findings are consistent with a wider role for sensory drive in the diversification of lineages with acoustic mating signals.     

Geographic variation in bird songs: examination of the effects of sympatric related species on the acoustic structure of songs

Birdsong evolution has influenced by various ecological and social factors. When related species that sing similar songs coexist, the acoustic properties of the songs of one or both species may shift, and the songs may diverge. We investigated geographic variation in the songs of the Japanese tit (Parus minor) and the varied tit (Poecile varius) in the Ryukyu Archipelago, Japan, whose islands harbor either one or both species. The songs of the two species exhibited similar structure, but acoustic measurements differed between them. For example, varied tits sang songs at higher frequency than Japanese tits did. The songs of both species varied geographically. At sites with higher relative densities of varied tits, Japanese tits sang lower frequency songs, indicating that in areas of coexistence, Japanese tits sang songs that had acoustically diverged from those of varied tits. Song variation in varied tits was not related to sympatry with Japanese tits. These asymmetric results suggest that the subordinate Japanese tit modified the acoustic characteristics of its song to avoid harassment by the dominant varied tit. We observed no effects of genetic divergence or local intraspecific density on Japanese tit or varied tit songs. This study used geographic variation to examine hypotheses of song evolution, and the results highlight the importance of character displacement.     

Rock wrens preferentially use song types that improve long distance signal transmission during natural singing bouts

When animals are capable of producing variable signals they may preferentially use some signal types over others. Among songbirds, individuals are known to alter song type form and usage patterns in contest and mating situations, but studies have not examined how song choice improves signal efficacy during broadcast song. For this study we investigated rock wren Salpinctes obsoletus song type use rates during natural singing bouts. We tested three hypotheses for adaptive song use during broadcast song: 1) birds improve signal content by increasing the use of high quality songs, 2) birds optimize for signal propagation by preferentially using songs that transmit well, and 3) birds maintain energy by reducing the use of costly songs. The study included 19 058 songs sung by 12 individuals, each of which had a measured song repertoire of between 52 and 117 song types which were produced at highly variable rates. Results indicated that rock wrens did not preferentially sing song types with shorter durations or fewer frequency switches, as would be expected if they selected song types to minimize delivery costs. They also did not favor songs with more rapid trills or more frequency switches, as would be expected if they adjusted song use primarily to indicate quality. Focal birds did preferentially sing significantly longer songs with lower bandwidths, lower frequencies, and slower trill rates. Results suggest that natural broadcast singing patterns are shaped more by the benefits of long distance transmission than by the benefits of advertising performance ability or the costs of song production.     

The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song

Understanding the divergence of behavioural signals in isolated populations is critical to knowing how certain barriers to gene flow can develop. For many bird species, songs are essential for conspecific recognition and mate choice. Measuring the rate of song divergence in natural populations is difficult, but translocations of endangered birds to isolated islands for conservation purposes can yield insights, as the age and source of founder populations are completely known. We found significant and rapid evolution in the structure and diversity of bird song in North Island saddlebacks, Philesturnus rufusater, in New Zealand, with two distinct lineages evolving in < 50 years. The strong environmental filters of serial translocations resulted in cultural bottlenecks that generated drift and reduced song variability within islands. This rapid divergence coupled with loss of song diversity has important implications for the behavioural evolution of this species, demonstrating previously unrecognised biological consequences of conservation management.     

Limited genetic differentiation between acoustically divergent populations of urban and rural silvereyes (Zosterops lateralis)

The bioacoustic attributes of vocalisations made by birds in urban environments often differ markedly from those of rural conspecifics. Whether such differences are result from genetic divergence between urban and rural populations, or from plasticity or cultural evolution of song remains poorly understood. Silvereyes (Zosterops lateralis) show evidence of acoustic adaptation to urban noise, modifying both their songs and calls in cities when compared to rural areas. We investigated whether these differences were associated with corresponding morphological and neutral genetic differences. Across six pairs of geographically separate urban and rural populations, all morphological traits measured were similar. Furthermore, genetic analyses of variation at nine microsatellite loci revealed high levels of genetic connectivity between populations, and similar levels of heterozygosity in both habitat types. Consistent directional shifts in song attributes of city birds across large geographic areas thus do not appear to be accompanied by associated morphological or neutral genetic divergence.     

Acoustic signals in insects: A reproductive barrier and a taxonomic character

In singing insects, the song is an important component of the specific mate recognition system (SMRS). In communities of sympatric singing species, there is a partitioning of communication channels, the so-called “acoustic niches.” Within one community, the songs of different species always differ in temporal or frequency characters, i.e. occupy different acoustic niches. However, conspecific songs do not always act as an interspecific reproductive barrier, despite always being a SMRS component. The species that do not communicate acoustically due to allopatry, different timing of vocalization, inhabiting different biotopes, or unmatched food specializations can produce similar songs while forming reproductively isolated communities. Individuals of different sexes need not only to recognize a conspecific mate but also to evaluate its “quality.” The close-range signal (courtship song) provides more opportunities for choosing the “best” male than does the distant signal (calling song). In many species of Orthoptera, courtship includes not only acoustic but also vibrational, visual, chemical, and mechanical signals. An analysis of cricket songs showed the courtship songs to be on average more elaborate and variable than the calling songs. At the same time, due to the difference in mating behavior between the two groups, the acoustic component of courtship is used for mate quality evaluation to a greater extent in grasshoppers than in crickets. The courtship songs of grasshoppers are generally more elaborate in temporal structure than cricket songs; moreover, they may be accompanied by visual displays such as movements of various body parts. Thus, song evolution in grasshoppers is more strongly driven by sexual selection than that in crickets. According to the reinforcement hypothesis, the premating barrier between hybridizing species becomes stronger in response to reduced hybrid fitness. However, our behavioral experiments with two groups of hybridizing grasshopper species did not confirm the reinforcement hypothesis. We explain this, firstly, by a low level of genetic incompatibility between the hybridizing species and secondly, by high hybrid fitness when attracting a mate. A high competitive capability of hybrids may be accounted for by attractiveness of new elements in hybrid courtship songs. When we divide similar forms based on their songs, we in fact distinguish biological species using the criterion of their reproductive isolation. Acoustic differences between species are usually greater than morphological ones. Therefore, song analysis allows one to determine the real status of doubtful species-rank taxa, to distinguish species in a medley of sibling forms, and to reveal cryptic species in the cases when morphological studies fail to provide a univocal result. At the same time, songs are subject to intraspecific variation the range of which is different in different groups. Therefore, it is necessary to study which degree of difference corresponds to the species level before interpreting the status of some forms based on song comparisons. Besides, song similarities cannot indicate conspecificity of acoustically isolated forms; on the other hand, song differences between these forms prove that they are full-rank species.     

Black‐capped chickadees Poecile atricapillus sing at higher pitches with elevated anthropogenic noise,but not with decreasing canopy cover

Several songbird species sing at higher frequencies (i.e. higher pitch) when anthropogenic noise levels are elevated. Such frequency shifting is thought to be an adaptation to prevent masking of bird song by anthropogenic noise. However, no study of this phenomenon has examined how vegetative differences between noisy and quiet sites influence frequency shifting. Variation in vegetative structure is important because the acoustic adaptation hypothesis predicts that birds in more open areas should also sing at higher frequencies. Thus, vegetative structure may partially explain the observation of higher frequency songs in areas with high levels of anthropogenic noise. To distinguish between frequency shifting due to noise or vegetative structure we recorded the songs of black‐capped chickadees Poecile atricapillus vocalizing in high and low noise sites with open and closed canopy forests. Consistent with the noise‐dependent frequency hypothesis, black‐capped chickadees sang at higher frequencies in high noise sites than in low noise sites. In contrast, birds did not sing at higher frequencies in sites with more open canopies. These results suggest that frequency shifting in chickadees is more strongly related to ambient noise levels than to vegetative structure. A second frequency measure, inter‐note ratio, was reduced at higher levels of canopy cover. We speculate that this may be due to a non‐random distribution of dominant males. In sum, our results support the hypothesis that some birds sing at higher frequencies to avoid overlap with anthropogenic noise, but suggest that vegetative structure may play a role in the modification of other song traits.     

Evolution of acoustic and visual signals in Asian barbets

The study of animal communication systems is an important step towards gaining greater understanding of the processes influencing diversification because signals often play an important role in mate choice and can lead to reproductive isolation. Signal evolution can be influenced by a diversity of factors such as biophysical constraints on the emitter, the signalling environment, or selection to avoid heterospecific matings. Furthermore, because signals can be costly to produce, trade‐offs may exist between different types of signals. Here, we apply phylogenetic comparative analyses to study the evolution of acoustic and visual signals in Asian barbets, a clade of non‐Passerine, forest‐dependent birds. Our results suggest that evolution of acoustic and visual signals in barbets is influenced by diverse factors, such as morphology and signalling environment, suggesting a potential effect of sensory drive. We found no trade‐offs between visual and acoustic signals. Quite to the contrary, more colourful species sing significantly longer songs. Song characteristics presented distinct patterns of evolution. Song frequency diverged early on and the rate of evolution of this trait appears to be constrained by body size. On the other hand, characteristics associated with length of the song presented evidence for more recent divergence. Finally, our results indicate that there is a spatial component to the evolution of visual signals, and that visual signals are more divergent between closely related taxa than acoustic signals. Hence, visual signals in these species could play a role in speciation or reinforcement of reproductive isolation following secondary contacts.     

Relationships of song structure to phylogenetic history,habitat, and morphology in the vireos,greenlets, and allies (Passeriformes: Vireonidae)

Acoustic signals show immense variation among passerines, and several hypotheses have been proposed to explain this diversity. In this study, we tested, for the first time, the relationships of song structure to phylogeny, habitat type, and morphology in the vireos and allies (Vireonidae). Every measure of song structure considered in this study had moderate and significant phylogenetic signal. Furthermore, two song-constraining morphological traits, bill shape and body mass, also exhibited significant phylogenetic signal. Song length showed the largest within-clade similarity; longer songs were highly conserved in part of the greenlet (Hylophilus) clade, whereas shorter songs characterized the remaining seven genera. We found no differences in song structure among vireonids living in different habitat types. However, vireonids with shorter, stouter bills and larger bodies sang songs with lower minimum and maximum peak frequency, compared with species with longer, thinner bills and smaller bodies. We conclude that Vireonidae song evolution is driven partially by phylogenetically conserved morphological traits. Our findings support the phylogenetic signal and morphological constraints hypotheses explaining structural diversity in avian acoustic signals.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.