Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Ability to alter song in two grassland songbirds exposed to simulated anthropogenic noise is not related to pre-existing variability

Organisms encounter noise naturally in the environment. However, increasing prevalence of human-caused noise seems to be resulting in behavioural changes in many animals that can affect survival and reproduction. Not all species react the same way to noise; some adjust their vocal signals while others do not. We hypothesized that species with more variability in their vocal signals would be better able to adjust their signals to be audible over anthropogenic noise. We tested this within a large-scale manipulative experiment by recording songs of two grassland songbirds, Baird’s sparrow (Ammodramus bairdii) and Savannah sparrow (Passerculus sandwichensis), both of which are found in areas increasingly affected by energy extraction noise. We compared these species because Savannah sparrows have more variability in their songs geographically and temporally compared to Baird’s sparrows. We recorded both species’ songs before, during and after high-fidelity playbacks of oil well drilling noise. Surprisingly, both species changed parts of their songs in the presence of noise (Baird’s sparrow usually decreasing frequency and Savannah sparrow increasing frequency) and these changes were not related to seasonal, song, or syllable variability. We suggest instead that acoustically heterogeneous environments may favour the evolution of species that are capable of adjusting their songs in response to variable ambient noise.     

Divergence in mating signals correlates with genetic distance and behavioural responses to playback

Animals use acoustic signals to defend resources against rivals and attract breeding partners. As with many biological traits, acoustic signals may reflect ancestry; closely related species often produce more similar signals than do distantly related species. Whether this similarity in acoustic signals is biologically relevant to animals is poorly understood. We conducted a playback experiment to measure the physical and vocal responses of male songbirds to the songs of both conspecific and allopatric‐congeneric animals that varied in their acoustic and genetic similarity. Our subjects were territorial males of four species of neotropical Troglodytes wrens: Brown‐throated Wrens (Troglodytes brunneicollis), Cozumel Wrens (T. beani), Clarion Wrens (T. tanneri) and Socorro Wrens (T. sissonii). Our results indicate that birds respond to playback of both conspecific and allopatric‐congeneric animals; that acoustic differences increase with genetic distance; and that genetic divergence predicts the strength of behavioural responses to playback, after removing the effects of acoustic similarity between subjects’ songs and playback stimuli. Collectively, these results demonstrate that the most distantly related species have the most divergent songs; that male wrens perceive divergence in fine structural characteristics of songs; and that perceptual differences between species reflect evolutionary history. This study offers novel insight into the importance of acoustic divergence of learned signals and receiver responses in species recognition.     

Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds

Many laboratories are conducting research using songbirds as their animal model. In particular, songbirds are widely used for studying the behavioural and neural mechanisms underlying vocal learning. Many researchers use wild-caught birds to conduct this research, although few studies of behaviour have been conducted to determine the effects of captive housing on these species. We investigated the vocal production pattern of wild-caught black-capped chickadees (Poecile atricapillus) over an entire season in laboratory housing. We documented the frequency of production of four vocalizations (fee-bee song, chick-a-dee calls, dee calls, and gargle calls) across seasons and diurnal pattern and compared the observed pattern of laboratory vocalizations to those previously observed and reported in the wild. Laboratory-housed chickadees had seasonal and diurnal vocal production shifts that were related to both photoperiodic changes (season) and diurnal pattern. For instance, there was significantly more fee-bee song in the spring than summer, autumn, and winter with the most fee-bee song occurring at spring dawn as seen in the wild. Our results also confirmed that the general pattern of vocalizations was consistent between wild and laboratory populations, with no significant differences for either the seasonal or diurnal pattern of fee-bee song production between populations. Differences between settings were observed in the pattern of chick-a-dee calls at dawn and sunset between field and laboratory populations. However, differences in the quantity of vocalization types between laboratory and wild populations suggest that housing conditions are influencing the normal vocal behavioural patterns.     

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the “gatekeepers” of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close‐range signals are as important as long‐distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.     

Courtship signals and mate choice of the flies of inbred Drosophila montana strains

We studied genetic variation in fly mating signals and mate choice in crosses within and between inbred strains of Drosophila montana. Male songs and the cuticular hydrocarbons of both sexes as well as some of the flies’ behavioural traits differed significantly between strains. This did not, however, cause sexual isolation between strains. In fact, courtship was shorter if the female was courted by a male of a foreign strain than when courted by their own male. Heterosis was found for courtship duration and the carrier frequency of male song. Diallel analysis of male song revealed additive genetic variation in four out of the five traits studied. Two traits showed dominance variation and one of these, carrier frequency, expressed unidirectional dominance with alleles for higher carrier frequency being dominant. Direction of dominance in carrier frequency was the same as the direction of sexual selection exercised by D. montana females on this trait, which suggests that sexual selection could be a driving force in the evolution of song towards a higher carrier frequency.     

Song rate as a signal of male aggressiveness during territorial contests in the wood warbler

Aggressive signaling is an important component in animal communication, as it provides an efficient mechanism for settling conflicts over resources between competitors. In songbirds, a number of singing behaviors have been proposed to be aggressive signals used in territory defense, including song rate. Although aggressive signaling in songbirds has received considerable research attention, adequate evidence for most putative aggressive signals is not available. In this study, we experimentally investigated whether the song rate of male wood warblers Phylloscopus sibilatrix is a signal of their aggressive intent in male–male interactions. We found that males responded differentially to simulated territorial intrusions depending on the song rate of an intruder. Moreover, males that continued to sing during territorial contests increased their song rates, and this behavior predicted the strength of aggressive escalation by the signaler. These results suggest that song rate is an aggressive signal during male–male interactions in the wood warbler. We also found high intra‐individual repeatability in the strength of aggressive response to simulated intrusions, likely reflecting differences in personality (aggressiveness) or quality of male wood warblers. We conclude that changes in singing rate may be an efficient mechanism of signaling immediate shifts in motivation of signalers during territorial contests, especially in species that lack large repertoires or have simple songs.     

Behavioural response to song and genetic divergence in two subspecies of white‐crowned sparrows (Zonotrichia leucophrys)

Divergence in sexual signals may drive reproductive isolation between lineages, but behavioural barriers can weaken in contact zones. Here, we investigate the role of song as a behavioural and genetic barrier in a contact zone between two subspecies of white‐crowned sparrows (Zonotrichia leucophrys). We employed a reduced genomic data set to assess population structure and infer the history underlying divergence, gene flow and hybridization. We also measured divergence in song and tested behavioural responses to song using playback experiments within and outside the contact zone. We found that the subspecies form distinct genetic clusters, and demographic inference supported a model of secondary contact. Song phenotype, particularly length of the first note (a whistle), was a significant predictor of genetic subspecies identity and genetic distance along the hybrid zone, suggesting a close link between song and genetic divergence in this system. Individuals from both parental and admixed localities responded significantly more strongly to their own song than to the other subspecies song, supporting song as a behavioural barrier. Putative parental and admixed individuals were not significantly different in their strength of discrimination between own and other songs; however, individuals from admixed localities tended to discriminate less strongly, and this difference in discrimination strength was explained by song dissimilarity as well as genetic distance. Therefore, we find that song acts as a reproductive isolating mechanism that is potentially weakening in a contact zone between the subspecies. Our findings also support the hypothesis that intraspecific song variation can reduce gene flow between populations.     

Bilateral Song Convergence in a Passerine Hybrid Zone: Genetics Contribute in One Species Only

Hybridization can drive the convergence of territorial and sexual signals. However, non-genetic processes such as competition, environment matching, or cultural transmission, also generate this pattern. We investigated the effect of hybridization on song convergence between two interspecifically territorial warblers in a moving hybrid zone. We confirmed song convergence in each species. Using an AFLP-based genetic index, we detected an effect of genetics on song convergence in Hippolais polyglotta, the expanding species. Evidence was weaker for H. icterina, the receding species. In moving zones, introgression is expected to be larger in the expanding species than in the receding. Thus, the asymmetric contribution of the genetic index to convergence was consistent with expectations for genetically determined traits in moving hybrid zones, and the observed introgression pattern of AFLP markers. However, the geographical location of individuals had an effect on song variation too when genetics was accounted for, suggesting that convergence also has non-genetic explanations. We examine the possible role of alternative processes to that of hybridization and discuss their conflicting effects on reinforcement and hybrid zone dynamics.     

Quality calls: phylogeny and biogeography of a new genus of neotropical katydid (Orthoptera: Tettigoniidae) with ultra pure-tone ultrasonics

This paper describes Artiotonus, a new genus of tropical katydid from Colombia and Ecuador. These acoustic ensiferans are represented by three species with a geographic distribution generally restricted to the rainforest of the Bolivar geosyncline of northwestern South America (Pacific). A phylogenetic analysis based on 28 morphological and six behavioural characters produced a tree (A. artius, (A. tinae, A. captivus)) with a consistency index of 0.9. All species are defined by a few autapomorphic changes. The most reliable character for identification is the temporal pattern of the calling song, suggesting a recent genetic divergence. Biogeographic analysis indicates that such genetic divergence began with geographic isolation produced before the Holocene transgression. Species of this genus are remarkable in that the calling song of males exhibits a narrow spectrum with a high quality factor (37–42), unusual values for such ultrasonic signals. A broad discussion on the evolution of tonal calls and pulse trains is offered.     

Comparative approaches to the avian song system

There is extensive diversity among the 4000 species of songbirds in different aspects of song behavior, including the timing of vocal learning, sex patterns of song production, number of songs that are learned (i.e., repertoire size), and seasonality of song behavior. This diversity provides unparalleled opportunities for comparative studies of the relationship between the structure and function of brain regions and song behavior. The comparative approach has been used in two contexts: (a) to test hypotheses about mechanisms of song control, and (b) to study the evolution of the control system in different groups of birds. In the first context, I review studies in which a comparative approach has been used to investigate sex differences in the song system, the relationship between the number of song types a bird sings and the size of the song nuclei, and seasonal plasticity of the song control circuits. In the second context, I discuss whether the vocal control systems of parrots and songbirds were inherited from a common ancestor or independently evolved. I also consider at what stage in the phylogeny of songbirds the hormone-sensitive forebrain circuit found in modern birds first evolved. I conclude by identifying directions for future research in which a comparative approach would be productive. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 517–531, 1997     

Acoustic but no genetic divergence in migratory and sedentary populations of blackcaps,Sylvia atricapilla

In songbirds, territorial songs are key regulators of sexual selection and are learned from conspecifics. The cultural transmission of songs leads to divergence in song characteristics within populations, which can ultimately lead to speciation. Many songbirds also migrate, and individual differences in migratory behaviours can influence population genetic structure and local song differentiation. Blackcaps, Sylvia atricapilla, exhibit versatile territorial songs and show diversity in migration behaviours. They therefore comprise a good model for investigating the relationships between migratory patterns, song variation, and genetic diversity. We studied a migratory population (two groups near Paris) and a sedentary population (three groups in Corsica). All of the birds were ringed and blood sampled to investigate genetic relatedness using 17 microsatellite loci. A detailed song analysis showed that this species has a complex repertoire (> 100 syllables), which required the development of a semi‐supervised method to classify different categories of syllables and compare sequences of syllables. Our analysis showed no genetic structuring among populations: individuals belonging to the same group were not genetically closer than those from different groups. However, we found a strong wingsize difference between sedentary and migratory populations. We also showed that geographical variations in songs rely at least on both syllable and sequence content. Unexpectedly, despite a higher turnover of individuals, migratory groups share as many syllables and sequences as sedentary groups, which raises interesting issues on song learning and the maintenance of dialects in migratory birds.     

Geographic variation and the evolution of song in Mesoamerican rufous‐naped wrens Campylorhynchus rufinucha

Speciation may be influenced by geographic variation in animal signals, particularly when those signals are important in reproductive decisions. Here, we describe patterns of geographic variation in the song of rufous‐naped wrens Campylorhynchus rufinucha. This species complex is a morphologically variable taxon confined to tropical dry forest areas from Mexico to northwestern Costa Rica. Morphological and genetic analyses suggest that there are at least three partially isolated groups within the complex, including a secondary‐contact zone in coastal western Chiapas between the subspecies C. r. humilus and C. r. nigricaudatus. Based on recordings throughout their geographic range, we investigate the effects of historical isolation on song structure and analyze whether genetic differences or climatic conditions explain observed patterns of variation. Our findings, based on a culturally‐transmitted and sexually‐selected trait, support the hypothesis that three evolutionary units exist within this taxon. Our results suggest that song differences between genetic groups were influenced by historical isolation. We report a strong relationship between vocal dissimilarity and genetic distance, suggesting that differences in vocal characteristics are probably affected by the same factors that drive genetic divergence. We argue that the evolution of song in this taxon is influenced by vicariant events, followed by accumulation of changes in song structure due to several possible factors: cultural drift in song structure; genetic drift in features related to song production; or natural selection acting on features that influence songs, such as body and beak size.     

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.     

No Correlation Between Song and Circulating Testosterone Levels During Multiple Broods in the Domesticated Canary (Serinus canaria)

In anticipation of the breeding season male songbirds of the temperate zones undergo gonadal recrudescence in early spring that lead to elevated circulating testosterone (T) levels, positively correlated with an increase in aggressive and song behaviour. However, besides seasonal changes there are also marked fluctuations of T levels and song production within the breeding season. In many species, T levels and singing activity drop after pairing or after the first clutch is laid. Domesticated canaries (Serinus canaria) are multiple‐brooded with an extended breeding season, and males continue to sing after egg‐laying. So far, studies have mainly focused on the seasonality of T levels and song behaviour whereas the pattern of change throughout the breeding period is unknown. Here, we focused on the first and on the last brood of the breeding season. We measured plasma T levels in males at the different breeding stages and assessed song characteristics of males at both times. T levels fluctuated significantly throughout brood 1, being highest during the nest building stage compared with egg‐laying and feeding of young. No such changes occurred during the last brood. Temporal song characteristics changed between brood 1 and brood 3 with song length being the main contributor to explain these changes. Our data suggest that T mainly plays a role in mate attraction and initial nesting site selection but that elevated levels are not necessary for subsequent breeding attempts. Furthermore, temporal song characteristics are maintained independently of T levels, suggesting a threshold effect. Our results demonstrate behavioural and physiological plasticity of domesticated canaries during the breeding season and are consistent with previous findings in wild songbirds.     

Song Feature Specific Analysis of Isolate Song Reveals Interspecific Variation in Learned Components

Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been thoroughly investigated in a few model species, resulting in a narrow view of birdsong learning. By extracting acoustic signals from published spectrograms, we have reexamined the findings of isolate studies with a universally applicable semi‐automated quantitative analysis regimen. When song features were analyzed in light of three different production aspects (respiratory, syringeal, and central programming of sequence), all three show marked interspecific variability in how close isolate song features are to normal. This implies that song learning mechanisms are more variable than is commonly recognized. Our results suggest that the interspecific variation shows no readily observable pattern reflecting phylogeny, which has implications for understanding the mechanisms behind the evolution of avian vocal communication. We emphasize that song learning in passerines provides an excellent opportunity to investigate the evolution of a complex, plastic trait from a phylogenetic perspective.     

MULTIPLE GENETIC LINKAGES BETWEEN FEMALE PREFERENCE AND MALE SIGNAL IN RAPIDLY SPECIATING HAWAIIAN CRICKETS

Diverging sexual communication systems can lead to the evolution of new species that no longer recognize each other as potential mates. The coevolution of male and female components of sexual communication is facilitated by physical linkage between genes underlying signals and preferences. By crossing two closely related Hawaiian crickets (Laupala kohalensis and Laupala paranigra) with vastly different song pulse rates and female preferences, and assessing segregation of songs and preferences among second generation backcrosses, we show a strong genetic correlation between song and preference variation. Furthermore, multiple, but not all, quantitative trait loci underlying song variation also predict female preferences. This physical linkage or pleiotropy may have facilitated the striking diversification of pulse rates observed among Laupala species in conjunction with one of the most rapid species radiations so far recorded.     

The genetics of speciation: genes of small effect underlie sexual isolation in the Hawaiian cricket Laupala

Sexual behaviours often evolve rapidly and are critical for sexual isolation. We suggest that coordinated sexual signals and preferences generate stabilizing selection, favouring the accumulation of many small‐effect mutations in sexual communication traits. Rapid radiation of a sexual behaviour used in signalling, song pulse rate, has been observed in the Hawaiian cricket genus Laupala. Using marker‐assisted introgression, we isolated five known quantitative trait loci (QTL) influencing species‐level differences in pulse rate from one species, L. paranigra, into a closely related species, L. kohalensis. All five QTL were found to have a significant effect on song and appear to be largely additive in backcross introgression lines. Furthermore, all effect sizes were small in magnitude. Our data provide support for the hypothesis that stabilizing selection on sexual signals in Laupala creates genetic conditions favourable to incremental divergence during speciation, through the evolution of alleles of minor rather than major phenotypic effects.     

Male response to historical and geographical variation in bird song

In many species, individuals discriminate among sexual signals of conspecific populations in the contexts of mate choice and male–male competition. Differences in signals among populations (geographical variation) are in part the result of signal evolution within populations (temporal variation). Understanding the relative effect of temporal and geographical signal variation on signal salience may therefore provide insight into the evolution of behavioural discrimination. However, no study, to my knowledge, has compared behavioural response to historical signals with response to current signal variation among populations. Here, I measured the response of male white-crowned sparrows (Zonotrichia leucophrys) to historical songs compared with current songs from their local population, a nearby non-local population and a distant population. Males responded most strongly to current local songs, less, but equally, to historical local and current non-local songs, and least to songs of the distant population. Moreover, response to both temporal and geographical variation in song was proportional to how much songs differed acoustically from current local songs. Signal evolution on an ecological time scale appears to have an effect on signal salience comparable to differences found between current neighbouring populations, supporting the idea that behavioural discrimination among learned signals of conspecific populations can evolve relatively rapidly.