Oscine Research Articles

Genome of an iconic Australian bird: High-quality assembly and linkage map of the superb fairy-wren (Malurus cyaneus).

The superb fairy-wren, Malurus cyaneus, is one of the most iconic Australian passerine species. This species belongs to an endemic Australasian clade, Meliphagides, which diversified early in the evolution of the oscine passerines. Today, the oscine passerines comprise almost half of all avian species diversity. Despite the rapid increase of available bird genome assemblies, this part of the avian tree has not yet been represented by a high-quality reference. To rectify that, we present the first high-quality genome assembly of a Meliphagides representative: the superb fairy-wren. We combined Illumina shotgun and mate-pair sequences, PacBio long-reads, and a genetic linkage map from an intensively sampled pedigree of a wild population to generate this genome assembly. Of the final assembled 1.07-Gb genome, 975Mb (90.4%) was anchored onto 25 pseudochromosomes resulting in a final superscaffold N50 of 68.11Mb. This high-quality bird genome assembly is one of only a handful which is also accompanied by a genetic map and recombination landscape. In comparison to other pedigree-based bird genetic maps, we find that the fairy-wren genetic map more closely resembles those of Taeniopygia guttata and Parus major maps, unlike the Ficedula albicollis map which more closely resembles that of Gallus gallus. Lastly, we also provide a predictive gene and repeat annotation of the genome assembly. This new high-quality, annotated genome assembly will be an invaluable resource not only regarding the superb fairy-wren species and relatives but also broadly across the avian tree by providing a novel reference point for comparative genomic analyses.

Female song in Costa's Hummingbird (Calypte costae)

ABSTRACT Bird song has been extensively studied in oscine passerines, but far less is known about song in hummingbirds, which are distantly related to passerines. Song is generally thought of as a male trait. Here we document song in 2 wild female Costa's Hummingbirds (Calypte costae) of 10 examined. Their vocalizations closely resembled male song and were produced, undirected, on territories just prior to the breeding season. Both birds were confirmed as female and not young males, which resemble females: one had an enlarged ovary, and the other laid eggs. Our results imply that at least some female hummingbirds may learn song as well as males and have similar song capacity as males. The function, if any, of female song was not immediately clear. Female song seemed rarer in this population than in males and thus easy to overlook. Presence of female song could also be an overlooked phenomenon in other hummingbird species.

Song performance is a condition‐dependent dynamic trait honestly indicating the quality of paternal care in the bull‐headed shrike

The good parent hypothesis in sexual selection predicts that if females can increase their fitness by mating with males who provide high‐quality parental care, then female preferences for male phenotypes honestly indicating the quality of paternal care will evolve. In order to test this hypothesis, we investigated correlations between male song, the timing of pair formation of males, male feeding rate, and reproductive success, in the bull‐headed shrike Lanius bucephalus (an altricial oscine passerine with biparental care). Analysis revealed that although the timing of pair formation was not correlated with most song characteristics (e.g. repertoire size), male morphological traits (e.g. tail length), or male territory size, it was negatively correlated with male singing tempo (i.e. the number of notes uttered per second). Those males that sang at higher speeds were in better body condition (i.e. body mass standardized by tarsus length3 was higher), fed their chicks frequently during the nestling period, and raised heavy chicks. These results show that in the bull‐headed shrike male singing tempo is a condition‐dependent dynamic trait honestly indicating the quality of paternal care, and strongly supports the good parent hypothesis.

Evolutionary origins of vocal mimicry in songbirds.

Vocal learning is an important behavior in oscines (songbirds). Some songbird species learn heterospecific sounds as well as conspecific vocalizations. The emergence of vocal mimicry is necessarily tied to the evolution of vocal learning, as mimicry requires the ability to acquire sounds through learning. As such, tracking the evolutionary origins of vocal mimicry may provide insights into the causes of variation in song learning programs among songbirds. We compiled a database of known vocal mimics that comprised 339 species from 43 families. We then traced the evolutionary history of vocal mimicry across the avian phylogeny using ancestral trait reconstruction on a dataset of oscine passerines for which vocalizations have been described. We found that the common ancestor to oscines was unlikely to mimic sounds, suggesting that song learning evolved with mechanisms to constrain learning to conspecific models. Mimicry then evolved repeatedly within the songbird clade, either through relaxation of constraints on conspecific learning or through selection for active vocal mimicry. Vocal mimicry is likely ancestral in only a handful of clades, and we detect many instances of independent origins of mimicry. Our analysis underscores the liability of vocal mimicry in songbirds, and highlights the evolutionary flexibility of song learning mechanisms.

Birdsong characteristics are related to fragment size in a neotropical forest

The oscine passerines, an avian suborder that comprises almost half of all bird species worldwide, learn their song primarily through cultural transmission. As the world's forests become increasingly fragmented and the population sizes of many forest-dwelling species decline, there may be increasingly restricted opportunities for the transmission of cultural information. However, the effects of forest fragmentation on birdsong have not been well documented. In this paper, we examine the relationship between forest fragment size and song characteristics for two forest bird species, an oscine passerine (orange-billed sparrow, Arremon aurantiirostris) that learns its song culturally, and a suboscine passerine (scale-crested pygmy tyrant, Lophotriccus pileatus) that does not. Recordings were taken from individuals in 12 premontane wet forest fragments ranging in size from approximately 1.4 ha–360 ha in southern Costa Rica. As predicted under the ‘cultural erosion’ hypothesis, we found that acoustic characteristics associated with song complexity such as the number of syllables per song and song duration decreased with decreasing fragment size for the oscine but not for the suboscine species. This study supports the idea that learned cultural elements are sensitive to fragment size and that cultural diversity should be considered along with other forms of biodiversity in the conservation of social learning species.

House Crow (Corvus splendens) Eradication Measures from eThekwini Municipality, KwaZulu-Natal, South Africa

Within the Province of KwaZulu-Natal, in South Africa, eThekwini Municipality intends to implement a Project aimed at eradicating the House Crow (Corvus splendens) from its jurisdiction. In terms of the National Environmental Management: Biodiversity Act (NEMBA), Act 10 of 2004, the species is listed as a Category 1a under the Invasive Alien Species (IAS) Regulations gazetted in July 2014 and as such requires immediate eradication efforts. The species belongs to a cosmopolitan family Corvidae, which has well over 120 species including oscine passerine birds such as crows, ravens, magpies, rooks, treepies etc. In line with legislation, eThekwini Municipality has implemented a number of large-scale programmes and projects aimed at controlling invasive alien species. In achieving this, the municipality has a strong belief in forming partnerships with relevant stakeholders, including academic institutions, neighboring municipalities, conservation authorities, conservancies, non-profit organizations, the private sector, provincial and national government departments etc.

A Scansorial Passerine Bird (Passeriformes, Certhioidea) from the Uppermost Lower Miocene of Eastern Siberia

A new scansorial passerine bird, Kischinskinia scandens gen. et sp. nov., from the uppermost Lower Miocene of the Tagay locality (Olkhon Island, Lake Baikal) is described based on a distal tarsometatarsal fragment. This is the first Asian member of the clade Certhioidea. A tibiotarsal fragment is also tentatively assigned to this taxon. Both bones display adaptations for climbing on a vertical surface. The find of a scansorial passerine bird of the clade Certhioidea is evidence of ecological similarity of Early Miocene avifaunas of southern Eastern Siberia and Western Europe, since a representative of Certhioidea showing a similar level of specialization was described from the Lower Miocene (MN3) of Germany. In addition, Kischinskinia scandens is the earliest reliable member of oscine passerines (Oscines) from Asia.

Age-related changes in song repertoire size and song type sharing in the Whinchat Saxicola rubetra

In many oscine passerines males’ songs, the repertoire size increases with age. At the same time it often remains unknown when and where males learn new songs. To infer the Whinchat Saxicola rubetra song learning strategy, we described and catalogued song-type repertoire, revealed age differences and examined song sharing strategies among neighbouring and distant males. We recorded song vocalizations of 40 males in a limited (104 ha) study plot during four years. Whinchats produce short and discrete songs with clear intersong pauses. In total 45 song types were allocated, the individual repertoire size averaged 23.5 ± 7.6 song types (range 9–34 song types). The males’ age significantly influenced the song-type repertoire size. The second calendar year (first breeding) males had a lower repertoire size than the older males. The majority of song types were shared by less than half of males in our sample. The Jaccard similarity indexes varied from 0.5 to 0.7. We could not find a relationship between males’ song sharing and geographic distances between their nests. We assume that Whinchat males learned new songs in the local population before territory establishment.

De-novo emergence of SINE retroposons during the early evolution of passerine birds

BackgroundPasseriformes (“perching birds” or passerines) make up more than half of all extant bird species. The genome of the zebra finch, a passerine model organism for vocal learning, was noted previously to contain thousands of short interspersed elements (SINEs), a group of retroposons that is abundant in mammalian genomes but considered largely inactive in avian genomes.ResultsHere we resolve the deep phylogenetic relationships of passerines using presence/absence patterns of SINEs. The resultant retroposon-based phylogeny provides a powerful and independent corroboration of previous sequence-based analyses. Notably, SINE activity began in the common ancestor of Eupasseres (passerines excluding the New Zealand wrens Acanthisittidae) and ceased before the rapid diversification of oscine passerines (suborder Passeri – songbirds). Furthermore, we find evidence for very recent SINE activity within suboscine passerines (suborder Tyranni), following the emergence of a SINE via acquisition of a different tRNA head as we suggest through template switching.ConclusionsWe propose that the early evolution of passerines was unusual among birds in that it was accompanied by de-novo emergence and activity of SINEs. Their genomic and transcriptomic impact warrants further study in the light of the massive diversification of passerines.

Comparative studies need to rely both on sound natural history data and on excellent statistical analysis.

We certainly agree with Schradin [1] that comparative studies need to use the best information available—as well as clear definitions, up-to-date statistical techniques and common sense. We have divided our response into two sections: the first dealing with Schradin's critique of our 2017 paper and the classification of the social organization of shrews; the second dealing with three general issues that his commentary raises. The paper that Schradin is commenting on [2] asks whether cooperative breeders (which we define as species where non-breeding helpers assist breeders to raise their young) in mammals are more commonly found in arid environments than monogamous species (defined as species where breeding pairs of males and females remain together for more than one season) from which cooperative breeders appear to be derived [3]. It shows that, as in birds, cooperative breeders tend to live in relatively arid habitats compared to monogamous species. As we describe below, these conclusions are unaffected by differences between our classification of the social organization of shrews and the classification suggested by Schradin. Schradin's first criticism is that the categorizations of shrews that we have used in this analysis were based on one paper on a single species. This is incorrect, for our categorization of shrews was based on more than 70 separate sources (see electronic supplementary material, appendix S1). When we published our dataset [4], we were required to reduce the associated reference list by the editors of the journal and, to comply, we removed around 75% of our 2000+ sources, often listing a single reference per species or group of species, and frequently using generic reviews for particular groups where these were available: for example, for many rodent species, we simply listed Wolff and Sherman's Rodent Societies [5], and …

Conservation genomics of the silktail (Aves: Lamprolia victoriae) suggests the need for increased protection of native forest on the Natewa Peninsula, Fiji

Effective conservation relies on accurate taxonomy, because we cannot protect what we do not know. Species limits among phenotypically differentiated and allopatrically distributed populations on Southwest Pacific islands are poorly understood. This likely has led to an underestimate of species richness in the Southwest Pacific, and, consequently, a biased application of conservation effort. The silktail Lamprolia victoriae is a bird species endemic to Fiji. Two subspecies are known from Vanua Levu and Taveuni Islands, but uncertainty remains whether they should be considered one or two species. If the latter, increased conservation effort is warranted to protect forest habitat where isolated populations occur only on the Natewa Peninsula. Here, we address this question by examining 8859 single nucleotide polymorphisms produced by restriction-site associated DNA sequencing. We find that the silktail is best considered two species, due to high genetic differentiation and low gene flow between the two subspecies. These differences match known phenotypic differences (size and plumage), as well as allopatric island distributions. We suggest that the silktail be used as an icon for conservation efforts of the heavily degraded forest habitats on the Natewa Peninsula. Finally, we reassess the divergence age estimates of Lamprolia and its relatives, Chaetorhynchus and Rhipidura, in light of new phylogenomic evidence from oscine passerines.

Changes in vocal repertoire of the Hawaiian crow, Corvus hawaiiensis, from past wild to current captive populations

For most avian species, social behaviour is critically important for survival and reproductive success. Many social behaviours in birds are culturally transmitted, and as bird populations decline across the globe, important elements of these behaviours may be lost. The Hawaiian crow or 'alalā, Corvus hawaiiensis, is a socially complex avian species that is currently extinct in the wild. As in other oscine passerines, vocalizations in the 'alalā may be culturally transmitted. We compared the vocal repertoire of three of the last four wild 'alalā pairs from the early 1990s to three current captive pairs on the Island of Hawai'i to determine how acoustic behaviour has been affected by changes in their social and physical environment. Over 18 h of recordings from wild breeding pairs were analysed and compared with 44 h from captive breeding pairs. Calls were placed into five putative behavioural categories: (1) alarm, (2) territorial broadcast, (3) aggression, (4) submission and (5) courtship. There was little difference in the overall number and diversity of call types among wild versus captive birds. However, the repertoire was significantly different. Territorial broadcast calls, common components of the wild repertoire, were absent from the captive repertoire. In addition, wild birds had twice the number of alarm calls and had a higher call rate than captive birds. Our results show how socially learned behaviours may change over relatively short periods for an entire species. Understanding how the vocal repertoire and the functional context of vocalizations change may provide useful information for ongoing efforts to reintroduce the 'alalā into the wild.

Tectonic collision and uplift of Wallacea triggered the global songbird radiation.

Songbirds (oscine passerines) are the most species-rich and cosmopolitan bird group, comprising almost half of global avian diversity. Songbirds originated in Australia, but the evolutionary trajectory from a single species in an isolated continent to worldwide proliferation is poorly understood. Here, we combine the first comprehensive genome-scale DNA sequence data set for songbirds, fossil-based time calibrations, and geologically informed biogeographic reconstructions to provide a well-supported evolutionary hypothesis for the group. We show that songbird diversification began in the Oligocene, but accelerated in the early Miocene, at approximately half the age of most previous estimates. This burst of diversification occurred coincident with extensive island formation in Wallacea, which provided the first dispersal corridor out of Australia, and resulted in independent waves of songbird expansion through Asia to the rest of the globe. Our results reconcile songbird evolution with Earth history and link a major radiation of terrestrial biodiversity to early diversification within an isolated Australian continent.

Elaborate Mimetic Vocal Displays by Female Superb Lyrebirds

Some of the most striking vocalizations in birds are made by males that incorporate vocal mimicry in their sexual displays. Mimetic vocalization in females is largely undescribed, but it is unclear whether this is because of a lack of selection for vocal mimicry in females, or whether the phenomenon has simply been overlooked. These issues are thrown into sharp relief in the superb lyrebird, Menura novaehollandiae, a basal oscine passerine with a lek-like mating system and female uniparental care. The spectacular mimetic song display produced by courting male lyrebirds is a textbook example of a sexually selected trait, but the vocalizations of female lyrebirds are largely unknown. Here, we provide the first analysis of the structure and context of the vocalizations of female lyrebirds. Female lyrebirds were completely silent during courtship; however, females regularly produced sophisticated vocal displays incorporating both lyrebird-specific vocalizations and imitations of sounds within their environment. The structure of female vocalizations varied significantly with context. While foraging, females mostly produced a complex lyrebird-specific song, whereas they gave lyrebird-specific alarm calls most often during nest defense. Within their vocal displays females also included a variety of mimetic vocalizations, including imitations of the calls of dangerous predators, and of alarm calls and song of harmless heterospecifics. Females gave more mimetic vocalizations during nest defense than while foraging, and the types of sounds they imitated varied between these contexts, suggesting that mimetic vocalizations have more than one function. These results are inconsistent with previous portrayals of vocalizations by female lyrebirds as rare, functionless by-products of sexual selection on males. Instead, our results support the hypotheses that complex female vocalizations play a role in nest defense and mediate female-female competition for breeding territories. In sum, this study reveals elaborate female vocal displays in a species widely depicted as an example of sexual selection for male extravagance, and thus highlights the hidden complexity of female vocalizations.

Female Song Occurs in Songbirds with More Elaborate Female Coloration and Reduced Sexual Dichromatism

Elaborate plumages and songs in male birds provide classic evidence for Darwinian sexual selection. However, trait elaboration in birds is not gender-restricted: female song has recently been revealed as a taxonomically-widespread trait within the songbirds (oscine Passerines), prompting increased research into likely functions and social/ecological correlates. Here we use phylogenetically-informed comparative analysis to test for an evolutionary association between female song and plumage color elaboration in songbirds. If there is an evolutionary trade-off between signaling modes, we predict a negative correlation between acoustic and visual elaboration. This trade-off hypothesis has been commonly proposed in males but has mixed empirical support. Alternatively, if song and plumage have similar or overlapping functions and evolve under similar selection pressures, we predict a positive correlation between female song and female plumage elaboration. We use published data on female song for 1,023 species of songbirds and a novel approach that allows for the reliable and objective comparison of color elaboration between species and genders. Our results reveal a significant positive correlation between female colorfulness and female song presence. In species where females sing, females (but not males) are on average more colorful – with concomitantly reduced average sexual dichromatism. These results suggest that female plumage and female song likely evolved together under similar selection pressures and that their respective functions are reinforcing. We discuss the potential roles of sexual versus social selection in driving this relationship, and the implications for future research on female signals.

The assembly and annotation of the complete Rufous-bellied thrush mitochondrial genome

Among known bird species, oscines are one of the few groups that produce complex vocalizations due to vocal learning. One of the most conspicuous oscine passerines in southeastern South America is the Rufous-bellied Thrush, Turdus rufiventris. The complete mitochondrial genome of this species was sequenced with the Illumina HiSeq platform (Illumina Inc., San Diego, CA), assembled using MITObim software and annotated by MITOS web server and Artemis software. This mitogenome contained 16 669 bases, organized as 13 protein-coding genes, 22 transfer RNAs, two ribosomal RNAs, and a control region (d-loop). The sequencing of the Rufous-bellied Thrush mitochondrial genome is of particular interest for better understanding of population genetics and phylogeography of the Turdidae family.

New perspectives in Amazonian bird vocal behavior

Neotropical region are known for its huge avian diversity and for the dominance of Sub-oscine or Tyranni passerines species. These species diversity are reflected in vocal communication and we will present here two examples of Brazilian Amazon forest of Tyranni species. Although the Tyranni are known for presenting a stereotyped song compared to Oscine passerines, we have found a species with a complex calls repertoire and other with a distinguished individual variation. The study area is the Ecological Park of Gunma, Santa Bárbara, Pará, Brazil, 50 km north of Belém. We performed playback experiments to define the vocalizations of Rusty-margined flycatcher Myiozetetes cayanensis, species that presents a complex repertoire of 15 different vocalizations, including a complex duet song. We also studied Lipaugus vociferans, a lekking bird, in which males perform conspicuous vocalizations in aggregations. We have analyzed songs of 19 individuals from six leks, considering the physical parameters (frequency bandwidth and temporal parameters) of the species-specific song. The results showed that it is possible to differentiate the individuals by song. These differences can represent an important function in individual recognition inside or between leks. These results show the necessity to investigate the high diversity of behavior in tropical habitats.

Evolution of leaf warbler songs (Aves: Phylloscopidae).

Songs in passerine birds are important for territory defense and mating. Speciation rates in oscine passerines are so high, due to cultural evolution, that this bird lineage makes up half of the extant bird species. Leaf warblers are a speciose Old-World passerine family of limited morphological differentiation, so that songs are even more important for species delimitation. We took 16 sonographic traits from song recordings of 80 leaf warbler taxa and correlated them with 15 potentially explanatory variables, pairwise, and in linear models. Based on a well-resolved molecular phylogeny of the same taxa, all pairwise correlations were corrected for relatedness with phylogenetically independent contrasts and phylogenetic generalized linear models were used. We found a phylogenetic signal for most song traits, but a strong one only for the duration of the longest and of the shortest element, which are presumably inherited instead of learned. Body size of a leaf warbler species is a constraint on song frequencies independent of phylogeny. At least in this study, habitat density had only marginal impact on song features, which even disappeared through phylogenetic correction. Maybe most leaf warblers avoid the deterioration through sound propagation in dense vegetation by singing from exposed perches. Latitudinal (and longitudinal) extension of the breeding ranges was correlated with most song features, especially verse duration (longer polewards and westwards) and complexity (lower polewards). Climate niche or expansion history might explain these correlations. The number of different element types per verse decreases with elevation, possibly due to fewer resources and congeneric species at higher elevations.

DNA barcoding and phylogenetic relationships in Timaliidae.

The Timaliidae, a diverse family of oscine passerine birds, has long been a subject of debate regarding its phylogeny. The mitochondrial cytochrome c oxidase subunit I (COI) gene has been used as a powerful marker for identification and phylogenetic studies of animal species. In the present study, we analyzed the COI barcodes of 71 species from 21 genera belonging to the family Timaliidae. Every bird species possessed a barcode distinct from that of other bird species. Kimura two-parameter (K2P) distances were calculated between barcodes. The average genetic distance between species was 18 times higher than the average genetic distance within species. The neighbor-joining method was used to construct a phylogenetic tree and all the species could be discriminated by their distinct clades within the phylogenetic tree. The results indicate that some currently recognized babbler genera might not be monophyletic, with the COI gene data supporting the hypothesis of polyphyly for Garrulax, Alcippe, and Minla. Thus, DNA barcoding is an effective molecular tool for Timaliidae species identification and phylogenetic inference.

Building the avian tree of life using a large-scale, sparse supermatrix

Birds are the most diverse tetrapod class, with about 10,000 extant species that represent a remarkable evolutionary radiation in which most taxa arose during a short period of time. There has been a tremendous increase in the amount of molecular data available from birds, and more than two-thirds of these species have some sequence data available. Here we assembled these available sequence data from birds to estimate a large-scale avian phylogeny. We performed an unconstrained maximum likelihood analysis of a sparse supermatrix comprising 22 nuclear loci and seven mitochondrial regions from 6714 species. We inferred a phylogeny with a backbone remarkably similar to that obtained by detailed analyses of multigene datasets, yet with the addition of thousands of more taxa. All orders were monophyletic with generally high support. While most families and genera were well supported, a number of them, especially within the oscine passerines, had little or no support. This likely reflects problems with the circumscription of these genera and families. Our results indicate that the amount of sequence data currently available is sufficient to produce a robust estimate of the avian tree of life using current methods of inference. The availability of a tree that is unconstrained by prior information, with branch lengths that have a direct connection to the underlying data, should be useful for comparative methods, taxonomic revisions, and prioritizing taxa that should be targeted for additional data collection.