Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Songbird species that display more-complex vocal learning are better problem-solvers and have larger brains.

Complex vocal learning, a critical component of human spoken language, has been assumed to be associated with more-advanced cognitive abilities. Tests of this hypothesis between individuals within a species have been inconclusive and have not been done across species. In this work, we measured an array of cognitive skills-namely, problem-solving, associative and reversal learning, and self-control-across 214 individuals of 23 bird species, including 19 wild-caught songbird species, two domesticated songbird species, and two wild-caught vocal nonlearning species. We found that the greater the vocal learning abilities of a species, the better their problem-solving skills and the relatively larger their brains. These conclusions held when controlling for noncognitive variables and phylogeny. Our results support a hypothesis of shared genetic and cognitive mechanisms between vocal learning, problem-solving, and bigger brains in songbirds.

Morphology, biochemistry and connectivity of Cluster N and the hippocampal formation in a migratory bird.

The exceptional navigational capabilities of migrating birds are based on the perception and integration of a variety of natural orientation cues. The "Wulst" in the forebrain of night-migratory songbirds contains a brain area named "Cluster N", which is involved in processing directional navigational information derived from the Earth´s magnetic field. Cluster N is medially joined by the hippocampal formation, known to retrieve and utilise navigational information. To investigate the connectivity and neurochemical characteristics of Cluster N and the hippocampal formation of migratory birds, we performed morphological and histochemical analyses based on the expression of calbindin, calretinin, parvalbumin, glutamate receptor type 1 and early growth response protein-1 in the night-migratory Garden warbler (Sylvia borin) and mapped their mutual connections using neuronal tract tracing. The resulting expression patterns revealed regionally restricted neurochemical features, which mapped well onto the hippocampal and hyperpallial substructures known from other avian species. Magnetic field-induced neuronal activation covered caudal parts of the hyperpallium and the medially adjacent hippocampal dorsomedial/dorsolateral subdivisions. Neuronal tract tracings revealed connections between Cluster N and the hippocampal formation with the vast majority originating from the densocellular hyperpallium, either directly or indirectly via the area corticoidea dorsolateralis. Our data indicate that the densocellular hyperpallium could represent a central relay for the transmission of magnetic compass information to the hippocampal formation where it might be integrated with other navigational cues in night-migratory songbirds.

Phenotypic selection on an ornamental trait is not modulated by breeding density in a pied flycatcher population.

Most studies of phenotypic selection in the wild have focussed on morphological and life-history traits and looked at abiotic (climatic) variation as the main driver of selection. Consequently, our knowledge of the effects of biotic environmental variation on phenotypic selection on sexual traits is scarce. Population density can be considered a proxy for the intensity of intrasexual and intersexual competition and could therefore be a key factor influencing the covariation between individual fitness and the expression of sexual traits. Here, we used an individual-based data set from a population of pied flycatchers (Ficedula hypoleuca) monitored over 24 years to analyze the effect of breeding density on phenotypic selection on dorsal plumage colouration, a heritable and sexually selected ornament in males of this species. Using the number of recruits as a fitness proxy, our results showed overall stabilizing selection on male dorsal colouration, with intermediate phenotypes being favoured over extremely dark and dull individuals. However, our results did not support the hypothesis that breeding density mediates phenotypic selection on this sexual trait. We discuss the possible role of other biotic factors influencing selection on ornamental plumage.

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.

Change in sexual signalling traits outruns morphological divergence across an ecological gradient in the post-glacial radiation of the songbird genus Junco.

The relative roles of natural and sexual selection in promoting evolutionary lineage divergence remains controversial and difficult to assess in natural systems. Local adaptation through natural selection is known to play a central role in promoting evolutionary divergence, yet secondary sexual traits can vary widely among species in recent radiations, suggesting that sexual selection may also be important in the early stages of speciation. Here, we compare rates of divergence in ecologically relevant traits (morphology) and sexually selected signalling traits (coloration) relative to neutral structure in genome-wide molecular markers and examine patterns of variation in sexual dichromatism to explore the roles of natural and sexual selection in the diversification of the songbird genus Junco (Aves: Passerellidae). Juncos include divergent lineages in Central America and several dark-eyed junco (J. hyemalis) lineages that diversified recently as the group recolonized North America following the last glacial maximum (ca. 18,000 years ago). We found an accelerated rate of divergence in sexually selected characters relative to ecologically relevant traits. Moreover, sexual dichromatism measurements suggested a positive relationship between the degree of colour divergence and the strength of sexual selection when controlling for neutral genetic distance. We also found a positive correlation between dichromatism and latitude, which coincides with the geographic axis of decreasing lineage age in juncos but also with a steep ecological gradient. Finally, we found significant associations between genome-wide variants linked to functional genes and proxies of both sexual and natural selection. These results suggest that the joint effects of sexual and ecological selection have played a prominent role in the junco radiation.

Can dominance genetic variance be ignored in evolutionary quantitative genetic analyses of wild populations?

Accurately estimating genetic variance components is important for studying evolution in the wild. Empirical work on domesticated and wild outbred populations suggests that dominance genetic variance represents a substantial part of genetic variance, and theoretical work predicts that ignoring dominance can inflate estimates of additive genetic variance. Whether this issue is pervasive in natural systems is unknown, because we lack estimates of dominance variance in wild populations obtained in situ. Here, we estimate dominance and additive genetic variance, maternal variance, and other sources of nongenetic variance in eight traits measured in over 9000 wild nestlings linked through a genetically resolved pedigree. We find that dominance variance, when estimable, does not statistically differ from zero and represents a modest amount (2-36%) of genetic variance. Simulations show that (1) inferences of all variance components for an average trait are unbiased; (2) the power to detect dominance variance is low; (3) ignoring dominance can mildly inflate additive genetic variance and heritability estimates but such inflation becomes substantial when maternal effects are also ignored. These findings hence suggest that dominance is a small source of phenotypic variance in the wild and highlight the importance of proper model construction for accurately estimating evolutionary potential.

Comparative Genomics Reveals Evolution of a Beak Morphology Locus in a High-Altitude Songbird.

The Ground Tit (Pseudopodoces humilis) has lived on the Qinghai-Tibet Plateau for ∼5.7 My and has the highest altitudinal distribution among all parids. This species has evolved an elongated beak in response to long-term selection imposed by ground-foraging and cavity-nesting habits, yet the genetic basis for beak elongation remains unknown. Here, we perform genome-wide analyses across 14 parid species and identify 25 highly divergent genomic regions that are significantly associated with beak length, finding seven candidate genes involved in bone morphogenesis and remolding. Neutrality tests indicate that a model allowing for a selective sweep in the highly conserved COL27A1 gene best explains variation in beak length. We also identify two nonsynonymous fixed mutations in the collagen domain that are predicted to be functionally deleterious yet may have facilitated beak elongation. Our study provides evidence of adaptive alleles in COL27A1 with major effects on beak elongation of Ps. humilis.

Mechanical and structural adaptations to migration in the flight feathers of a Palaearctic passerine.

Current avian migration patterns in temperate regions have been developed during the glacial retreat and subsequent colonization of the ice-free areas during the Holocene. This process resulted in a geographic gradient of greater seasonality as latitude increased that favoured migration-related morphological and physiological (co)adaptations. Most evidence of avian morphological adaptations to migration comes from the analysis of variation in the length and shape of the wings, but the existence of intra-feather structural adjustments has been greatly overlooked despite their potential to be under natural selection. To shed some light on this question, we used data from European robins Erithacus rubecula overwintering in Campo de Gibraltar (Southern Iberia), where sedentary robins coexist during winter with conspecifics showing a broad range of breeding origins and, hence, migration distances. We explicitly explored how wing length and shape, as well as several functional (bending stiffness), developmental (feather growth rate) and structural (size and complexity of feather components) characteristics of flight feathers, varied in relation to migration distance, which was estimated from the hydrogen stable isotope ratios of the summer-produced tail feathers. Our results revealed that migration distance not only favoured longer and more concave wings, but also promoted primaries with a thicker dorsoventral rachis and shorter barb lengths, which, in turn, conferred more bending stiffness to these feathers. We suggest that these intra-feather structural adjustments could be an additional, largely unnoticed, adaptation within the avian migratory syndrome that might have the potential to evolve relatively quickly to facilitate the occupation of seasonal environments.

Migrant and resident female songbirds differ in gonadal response to upstream stimulation during seasonal sympatry.

Timing of seasonal reproduction is driven by environmental cues acting on the hypothalamic-pituitary-gonadal (HPG) axis. Groups of individuals, or populations, of the same species can exhibit different phenology despite facing similar environmental cues or living in the same habitat (i.e., seasonal sympatry). The mechanisms giving rise to population-level differences in reproductive timing are not fully understood, particularly for females. We studied the dark-eyed junco, a songbird with migratory and sedentary (i.e., resident) populations that live in overlapping distributions during winter. In early spring, residents initiate breeding and associated behaviors, including territory establishment and formation of pair bonds, while migrants prepare to depart for their breeding grounds. We tested whether migrant and resident hormonal response to upstream hormonal stimulation differed during this time period. We collected blood from free-living females in early spring, and challenged them with repeated gonadotropin-releasing hormone (GnRH) injections to measure testosterone (T) response. We predicted that if migrants are less sensitive to upstream stimulation than residents, then they would exhibit lower response to the repeated GnRH challenges in migrants. We found that migrant and resident females both responded to an initial challenge by elevating T, but residents responded more robustly, indicating that the ovary plays a role in population-level differences in reproductive timing. We also found that migrants and residents attenuated their response to repeated challenges, and did not differ from one another in final T levels. We speculate that the explanation for the generally reduced T response after repeated GnRH injections need not be the same for migrants and residents, but possible explanations include suppression of upstream stimulation owing to negative feedback after the initial injection oraromatization of T to estradiol between sampling time points. We suggest that future studies experimentally explore how the ovarian response to upstream stimulation changes during the transition to reproduction.

The vocal organ of hummingbirds shows convergence with songbirds.

How sound is generated in the hummingbird syrinx is largely unknown despite their complex vocal behavior. To fill this gap, syrinx anatomy of four North American hummingbird species were investigated by histological dissection and contrast-enhanced microCT imaging, as well as measurement of vocalizations in a heliox atmosphere. The placement of the hummingbird syrinx is uniquely located in the neck rather than inside the thorax as in other birds, while the internal structure is bipartite with songbird-like anatomical features, including multiple pairs of intrinsic muscles, a robust tympanum and several accessory cartilages. Lateral labia and medial tympaniform membranes consist of an extracellular matrix containing hyaluronic acid, collagen fibers, but few elastic fibers. Their upper vocal tract, including the trachea, is shorter than predicted for their body size. There are between-species differences in syrinx measurements, despite similar overall morphology. In heliox, fundamental frequency is unchanged while upper-harmonic spectral content decrease in amplitude, indicating that syringeal sounds are produced by airflow-induced labia and membrane vibration. Our findings predict that hummingbirds have fine control of labia and membrane position in the syrinx; adaptations that set them apart from closely related swifts, yet shows convergence in their vocal organs with those of oscines.

The neurobiology of innate, volitional and learned vocalizations in mammals and birds.

Vocalization is an ancient vertebrate trait essential to many forms of communication, ranging from courtship calls to free verse. Vocalizations may be entirely innate and evoked by sexual cues or emotional state, as with many types of calls made in primates, rodents and birds; volitional, as with innate calls that, following extensive training, can be evoked by arbitrary sensory cues in non-human primates and corvid songbirds; or learned, acoustically flexible and complex, as with human speech and the courtship songs of oscine songbirds. This review compares and contrasts the neural mechanisms underlying innate, volitional and learned vocalizations, with an emphasis on functional studies in primates, rodents and songbirds. This comparison reveals both highly conserved and convergent mechanisms of vocal production in these different groups, despite their often vast phylogenetic separation. This similarity of central mechanisms for different forms of vocal production presents experimentalists with useful avenues for gaining detailed mechanistic insight into how vocalizations are employed for social and sexual signalling, and how they can be modified through experience to yield new vocal repertoires customized to the individual's social group. This article is part of the theme issue 'What can animal communication teach us about human language?'

Characteristics of song, brain-anatomy and blood androgen levels in spontaneously singing female canaries.

Females of many northern temperate songbird species sing sporadically. However, detailed descriptions of female song are rare. Here we report a detailed analysis of song in a small number of spontaneously-singing female domesticated canaries (Serinus canaria) under non-breeding, laboratory conditions in a large population of domesticated birds. In-depth analysis showed that these females sang rarely, and the spontaneous songs varied between and within birds over time. Furthermore, spontaneous female songs were distinct from songs of testosterone-induced singing female canaries and from songs of male canaries in both temporal and spectral features. Singing females had significantly elevated plasma androgen levels and a larger size of the major song controlling brain nuclei HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) than non-singing females housed under similar conditions. The sporadically observed production of song and accompanying differences in brain anatomy in female canaries may thus depend on minute intraspecific differences in androgen levels.

A novel cellular structure in the retina of insectivorous birds.

The keen visual systems of birds have been relatively well-studied. The foundations of avian vision rest on their cone and rod photoreceptors. Most birds use four cone photoreceptor types for color vision, a fifth cone for achromatic tasks, and a rod for dim-light vision. The cones, along with their oil droplets, and rods are conserved across birds - with the exception of a few shifts in spectral sensitivity - despite taxonomic, behavioral and ecological differences. Here, however, we describe a novel photoreceptor organelle in a group of New World flycatchers (Empidonax spp.) in which the traditional oil droplet is replaced with a complex of electron-dense megamitochondria surrounded by hundreds of small, orange oil droplets. The photoreceptors with this organelle were unevenly distributed across the retina, being present in the central region (including in the fovea), but absent from the retinal periphery and the area temporalis of these insectivorous birds. Of the many bird species with their photoreceptors characterized, only the two flycatchers described here (E. virescens and E. minimus) possess this unusual retinal structure. We discuss the potential functional significance of this unique sub-cellular structure, which might provide an additional visual channel for these small predatory songbirds.

A songbird compensates for wing molt during escape flights by reducing the molt gap and increasing angle of attack.

During molt, birds replace their feathers to retain feather quality and maintain flight performance. However, wing gaps inherent of this process can also reduce flight capacities, which could be detrimental when foraging or escaping predators. Still, many bird species will not cease their normal activities when molting. In this study, we investigated whether and how birds adjust their escape flight behavior to compensate for the reduction in performance when flying with wing gaps. Using stereoscopic high-speed videography, we filmed 146 upward-directed escape flights of 19 and 22 pied flycatchers (Ficedula hypoleuca) with and without simulated molt gaps, respectively. We then reconstructed the three-dimensional body and wing movements throughout each maneuver. By comparing flights with and without gaps, we determined how wing molt gaps affected wing morphology and escape flight performance, and how the birds adjusted their flight kinematics in order to negate possible negative aerodynamic effects. Our manipulations resulted in a lower second moment of area of the wings, but flight speed and net aerodynamic force production did not differ between the two groups. We found that in manipulated birds, the size of the gap was reduced as the flight feathers adjacent to the gap had moved towards each other. Moreover, the experimental decrease in second moment of area was associated with an increase in angle of attack, whereas changes in wingbeat-induced speeds were associated with variations in aerodynamic force production. This suggests that the control of escape flight in molting birds might be modular, allowing relatively simple flight control, thus reducing the burden on the neuro-muscular flight control system.

Rapid morphological change of nonnative frugivores on the Hawaiian island of O'ahu.

Novel ecosystems have become widespread created, in part, by the global spread of species. The nonnative species in these environments can be under intense evolutionary pressures that cause rapid morphological change, which can then influence species interactions. In Hawaii, much of the native frugivore community is extinct, replaced by nonnative bird species. Here, we determined if the passerine species of the nonnative frugivore community on O'ahu have morphologically diverged from their native ranges. We compared a variety of traits, all important for frugivory, between museum specimens from the species' native ranges to wild individuals from O'ahu. All four species tested exhibited significant divergence ranging in magnitude from 2.3% to 13.0% difference in at least two traits. Using a method developed from quantitative genetics, we found evidence that a mixture of nonadaptive and adaptive processes worked in concert to create the observed patterns of divergence. Our results suggest that rapid morphological change is occurring and, based on the traits measured, that these changes may influence seed dispersal effectiveness. As these species are largely responsible for seed dispersal on the island, the rapid morphological change of these species can influence the stability and maintenance of plant communities on O'ahu.

From the Himalayas to a continental Island: Integrative species delimitation in the Brownish-flanked Bush Warbler Horornis fortipes complex.

As species serve as basic units of study in many fields of biology, assessments of species limits are fundamental for such studies. Here, we used a multilocus dataset and different coalescent-based methods to analyze species delimitation and phylogenetic relationships in the Brownish-flanked Bush Warbler Horornis fortipes complex, which is widespread in the Sino-Himalayan region. We also examined the vocal and morphometric divergence within this complex. Our genetic results suggested that Horornis fortipes is composed of at least three independently evolving lineages, which diverged 1.1-1.8 million years ago. However, these lineages have hardly diverged in song or morphometrics and only very slightly in plumage. Our result indicate that there are three incipient species in Horonis fortipes complex diverged in central Himalayas and Hengduan Mountains, but not between the continent and Taiwan island.

Effect of barriers and distance on song, genetic, and morphological divergence in the highland endemic Timberline Wren (Thryorchilus browni, Troglodytidae).

Populations may become isolated by distance, geographic barriers or both. Isolated populations often diverge in behavioral, morphological and genetic traits as a result of reduced inter-population gene flow. Highland species commonly present naturally fragmented distributions that confine populations to the highest mountain peaks, isolated by mountain passes and distance. The endemic Timberline Wren (Thryorchilus browni) inhabits the highlands of the Talamanca mountain range, including western Panama, and the highest peak in the Central Volcanic mountain range of Costa Rica. Using microsatellites and song recordings we studied the effect of a geographic barrier and distance on song, genetic and morphological divergence among four populations in Costa Rica. A lowland mountain pass resulted in the largest genetic, vocal, and morphological (bill length) differences among populations, likely due to reduce the gene flow. Cultural drift and assortative mating by females selecting songs from their own population likely accentuates the effect of isolation and limited gene flow between populations. This pattern of population divergence has been found in other Neotropical highland birds, but over larger geographical scales. We conclude that mountain passes and distance both reduce gene flow between populations in recently-isolated highland species with restricted distributions.

The effect of early life conditions on song traits in male dippers (Cinclus cinclus).

Song complexity and singing frequency in male birds are shaped by female choice; they signal male quality because song is costly to develop and produce. The timing of song learning and the development of the brain structures involved occur during a period when chicks are exposed to a number of potential stressors. The quality and quantity of song produced by adults may therefore reflect the level of stress experienced during early life, a theory known as the 'developmental stress hypothesis'. We tested this hypothesis using song recordings and life-history data from an individually marked, long-term study population of wild dippers (Cinclus cinclus). The extent to which early life conditions predict adult song traits was investigated using natal brood size as a measure of sibling competition; the rate of provisioning by parents as a proxy for nutritional stress; and residuals of the linear regression between body mass and tarsus length as a measure of nestling condition. The syllable diversity in the songs of adult males was positively correlated with their body condition as nestlings, but there was no significant correlation with either provisioning rate or brood size. Provisioning rate did, however, predict song rate; males in relatively poor condition as nestlings or those raised in smaller broods which were fed more frequently by their parents sang at a higher rate in adulthood. These results support the developmental stress hypothesis and provide some of the first evidence from a wild bird of how the conditions experienced during early life impact adult song. Song traits may therefore provide females with information regarding both the current condition and developmental history of males.

A wood-warbler produced through both interspecific and intergeneric hybridization.

Hybridization between divergent taxa can provide insight into the breakdown of characters used in mate choice, as well as reproductive compatibility across deep evolutionary timescales. Hybridization can also occur more frequently in declining populations, as there is a smaller pool of conspecific mates from which to choose. Here, we report an unusual combination of factors that has resulted in a rare, three-species hybridization event among two genera of warblers, one of which is experiencing significant population declines. We use bioacoustic, morphometric and genetic data, to demonstrate that an early generation female hybrid between a golden-winged warbler (Vermivora chrysoptera) and a blue-winged warbler (V. cyanoptera) went on to mate and successfully reproduce with a chestnut-sided warbler (Setophaga pensylvanica). We studied the product of this event-a putative chrysoptera × cyanoptera × pensylvanica hybrid-and show that this male offspring sang songs like S. pensylvanica, but had morphometric traits similar to Vermivora warblers. The hybrid's maternal parent had V. chrysoptera mitochondrial DNA and, with six plumage-associated loci, we predicted the maternal parent's phenotype to show that it was likely an early generation Vermivora hybrid. That this hybridization event occurred within a population of Vermivora warblers in significant decline suggests that females may be making the best of a bad situation, and that wood-warblers in general have remained genetically compatible long after they evolved major phenotypic differences.