Martin Päckert

PHYLOGENETIC SIGNAL IN THE SONG OF CRESTS AND KINGLETS (AVES: REGULUS)

Abstract Territorial song structures are often the most prominent characters for distinguishing closely related taxa among songbirds. Learning processes may cause convergent evolution of passerine songs, but phylogenetic information of acoustic traits can be investigated with the help of molecular phylogenies, which are not affected by cultural evolutionary processes. We used a phylogeny based on cytochrome b sequences to trace the evolution of territorial song within the genus Regulus. Five discrete song units are defined as basic components of regulid song via sonagraphic measurements. Traits of each unit are traced on a molecular tree and a mean acoustic character difference between taxon pairs is calculated. Acoustic divergence between regulid taxa correlates strongly with genetic distances. Syntax features of complete songs and of single units are most consistent with the molecular data, whereas the abundance of certain element types is not. Whether song characters are innate or learned was interpreted using hand-reared birds in aviary experiments. We found that convergent character evolution seems to be most probable for learned acoustic traits. We conclude that syntax traits of whole verses or subunits of territorial song, especially innate song structures, are the most reliable acoustic traits for phylogenetic reconstructions in Regulus.

Phylogeny of long-tailed tits and allies inferred from mitochondrial and nuclear markers (Aves: Passeriformes, Aegithalidae)

In this paper we provide a molecular phylogeny based on three mitochondrial and three nuclear markers for all long-tailed tit species of the genus Aegithalos including several doubtful subspecies (17 taxa) plus three close allies of SE Asian Leptopoecile and North American Psaltriparus. Genus Aegithalos is divided into three major clades, two of them showing only minor differentiation. Separation of two mitchondrial haploytpe clusters in the N Palearctic Long-tailed Tit, Ae. caudatus, was dated back to the Late Pleistocene, however, descendants from both lineages underwent a rapid post-Pleistocene range expansion and largely mixed over the entire distribution area. The Chinese populations of the glaucogularis subspecies group represent a slightly earlier Pleistocene split from the Ae. caudatus clade. Genetic differentiation among several doubtful SE Asian species taxa on the sister clade of the latter N Palearctic/Chinese clade matches the intraspecific differentiation within Ae. caudatus. Unexpectedly, cytochrome-b distances among Himalayan Ae. iouschistos (including the subspecies bonvaloti from China and sharpei from Myanmar) and the Chinese endemic Ae. fuliginosus range at approximately 0.5% and apparently all these extant populations separated only very recently during late Pleistocene times, too. W Himalayan Ae. niveogularis clearly appeared as the sister species of the latter taxon assemblage. Unlike the two latter major clades, Ae. concinnus shows strong intraspecific differentiation with cyt-b distances as high as 6% among two Himalayan populations of ssp. iredalei, ssp. manipurensis from Myanmar and a fourth lineage from SW and SC China including ssp. talifuensis and nominate concinnus. A sister-group relationship between all Ae. concinnus and Ae. leucogenys was strongly supported. N American bushtits of genus Psaltriparus represent the sister clade to Palearctic genus Aegithalos, including a clear split between the minimus and the plumbeus subspecies group which was again dated back to Pleistocene times. The two tit-warbler species of genus Leptopoecile are strongly differentiated from one another and represent an early split from the Aegithalidae tree.

A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group

Quaternary climatic oscillations have been considered decisive in shaping much of the phylogeographic structure around the Mediterranean Basin. Within this paradigm, peripheral islands are usually considered as the endpoints of the colonization processes. Here, we use nuclear and mitochondrial markers to investigate the phylogeography of the blue tit complex (blue tit Cyanistes caeruleus, Canary blue tit C. teneriffae and azure tit C. cyanus), and assess the role of the Canary Islands for the geographic structuring of genetic variation. The Canary blue tit exhibits strong genetic differentiation within the Canary Islands and, in combination with other related continental species, provides an ideal model in which to examine recent differentiation within a closely related group of continental and oceanic island avian species. We analysed DNA sequences from 51 breeding populations and more than 400 individuals in the blue tit complex. Discrepancies in the nuclear and mitochondrial gene trees provided evidence of a complex evolutionary process around the Mediterranean Basin. Coalescent analyses revealed gene flow between C. caeruleus and C. teneriffae suggesting a dynamic process with multiple phases of colonization and geographic overlapping ranges. Microsatellite data indicated strong genetic differentiation among the Canary Islands and between the Canary archipelago and the close continental areas, indicating limited contemporary gene flow. Diversification of the blue tit complex is estimated to have started during the early Pliocene (≈ 5 Ma), coincident with the end of Messinian salinity crisis. Phylogenetic analyses indicated that the North African blue tit is derived from the Canary blue tits, a pattern is avian ‘back colonization’ that contrasts with more traditionally held views of islands being sinks rather than sources.

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.

Molecular phylogeny of Old World swifts (Aves: Apodiformes, Apodidae, Apus and Tachymarptis) based on mitochondrial and nuclear markers.

We provide a molecular phylogeny for Old World swifts of genera Apus and Tachymarptis (tribe Apodini) based on a taxon-complete sampling at the species level. Phylogenetic reconstructions were based on two mitochondrial (cytochrome b, 12S rRNA) and three nuclear markers (introns of fibrinogen and glyceraldehyde 3-phosphate dehydrogenase plus anonymous marker 12884) while the myoglobin intron 2 did not show any intergeneric variation or phylogenetic signal among the target taxa at all. In contrast to previous hypotheses, the two genera Apus and Tachymarptis were shown as reciprocally monophyletic in all reconstructions. Apus was consistently divided into three major clades: (1) East Asian clade of A. pacificus and A. acuticauda, (2) African-Asian clade of A. caffer, A. batesi, A. horus, A. affinis and A. nipalensis, (3) African-Palearctic clade of eight currently accepted species among which sequences of A. apus and A. pallidus clustered in a terminal crown clade. Phylogenetic signal of all four nuclear markers was extremely shallow within and among species of tribe Apodini and even among genera, such that intra- and intergeneric relationships of Apus, Tachymarptis and Cypsiurus were poorly resolved by nuclear data alone. Four species, A. pacificus, A. barbatus, A. affinis and A. caffer were consistently found to be paraphyletic with respect to their closest relatives and possible taxonomic consequences are discussed without giving particular recommendations due to limitations of sampling. Incomplete mitochondrial lineage sorting with cytochrome-b haplotypes shared among species and across large geographic distances was observed in two species pairs: A. affinis/A. nipalensis and A. apus/A. pallidus. Mitochondrial introgression caused by extant or past gene flow was ruled out as an explanation for the low interspecific differentiation in these two cases because all nuclear markers appeared to be highly unsorted among Apus species, too. Apparently, the two extant species pairs originated from very recent dispersal and/or speciation events. The currently accepted superspecies classification within Apus was not supported by our results.

Song dialects on the Atlantic islands: goldcrests of the Azores (Regulus regulus azoricus, R. r. sanctae-mariae, R. r. inermis)

Territorial songs in island populations of songbirds are often highly divergent from those of neighbouring continental relatives. This is shown for the three goldcrest subspecies (Regulus regulus azoricus, R. r. sanctae-mariae and R. r. inermis) endemic on six islands of the Azorean archipelago. All investigated populations display a high intra- and inter-individual acoustic variation. On each island, up to six different song types have been found; and a single male sings up to three types. In contrast, all northwestern European populations of R. r. regulus and R. r. anglorum share only a single song type. In playback experiments, none of 18 tested dialect songs of Azorean goldcrests evoked notable territorial reaction in German and Czech goldcrest males (ssp. regulus). Two differing dialect groups of the goldcrest can be distinguished on the Azores. Populations of the eastern islands, São Miguel and Santa Maria, share common song types which are not found on the islands of the central and western groups. Dialect repertoires on the westernmost islands, Flores, Faial and Pico, are dominated by a different song type. In the geologically younger western crater of São Miguel, both western and eastern song types coexist. Acoustic similarities to a population from neighbouring Terceira suggest the western part of São Miguel as the origin for the westward expansion of R. regulus on the Azores.

Evolutionary history of passerine birds (Aves: Passeriformes) from the Qinghai–Tibetan plateau: from a pre-Quarternary perspective to an integrative biodiversity assessment

As one of the most prominent topographical features on Earth, the Qinghai–Tibetan plateau (QTP) underwent a long and complex history of the QTP uplift from the collision of the Indian and the Eurasian plates to the present. At its southern and southeastern margins, it is flanked by the most significant hotspots of organismic diversity of the northern hemisphere (including birds), the Sino-Himalayan mountain forests. In contrast, the central plateau region itself harbours species-poor communities but also a good number of endemics that presumably evolved from rather ancient (pre-Pleistocene) phylogenetic lineage splits. We discuss the evolutionary history of QTP passerines from a twofold perspective including examples from our own research. First, we provide an overview of those alpine QTP endemics that represent late Miocene and Pliocene lineage splits, i.e. early colonisations to the central alpine QTP region. As an example, true rosefinches (genus Carpodacus) presumably evolved from a forested eastern QTP centre of origin and colonised the (semi-)open plateau habitats several times independently. Second, we discuss younger speciation events corresponding to phylogeographic east–west divides along the southern QTP margin. A multidisciplinary approach combining genetic, bioacoustic and morphological markers shed new light on the phylogenetic relationships of Pnoepyga wren babblers and on the intraspecific subdivision of the Buff-barred Warbler (Phylloscopus pulcher).

North African hybrid sparrows (Passer domesticus, P. hispaniolensis) back from oblivion – ecological segregation and asymmetric mitochondrial introgression between parental species

Abstract A stabilized hybrid form of the house sparrow (Passer domesticus) and the Spanish sparrow (P. hispaniolensis) is known as Passer italiae from the Italian Peninsula and a few Mediterranean islands. The growing attention for the Italian hybrid sparrow and increasing knowledge on its biology and genetic constitution greatly contrast the complete lack of knowledge of the long‐known phenotypical hybrid sparrow populations from North Africa. Our study provides new data on the breeding biology and variation of mitochondrial DNA in three Algerian populations of house sparrows, Spanish sparrows, and phenotypical hybrids. In two field seasons, the two species occupied different breeding habitats: Spanish sparrows were only found in rural areas outside the cities and bred in open‐cup nests built in large jujube bushes. In contrast, house sparrows bred only in the town centers and occupied nesting holes in walls of buildings. Phenotypical hybrids were always associated with house sparrow populations. House sparrows and phenotypical hybrids started breeding mid of March, and most pairs had three successive clutches, whereas Spanish sparrows started breeding almost one month later and had only two successive clutches. Mitochondrial introgression is strongly asymmetric because about 75% of the rural Spanish sparrow population carried house sparrow haplotypes. In contrast, populations of the Italian hybrid form, P. italiae, were genetically least diverse among all study populations and showed a near‐fixation of house sparrow haplotypes that elsewhere were extremely rare or that were even unique for the Italian Peninsula. Such differences between mitochondrial gene pools of Italian and North African hybrid sparrow populations provide first evidence that different demographic histories have shaped the extant genetic diversity observed on both continents.

Genome-wide data help identify an avian species-level lineage that is morphologically and vocally cryptic

Species identification has traditionally relied on morphology. However, morphological conservatism can lead to a high incidence of cryptic species, as characters other than morphological ones can be biologically important. In birds, the combined application of bioacoustic and molecular criteria has led to an avalanche of cryptic species discoveries over the last two decades in which findings of deep vocal differentiation have usually been corroborated by molecular data or vice versa. In this study, we use genome-wide DNA data to uncover an unusual case of cryptic speciation in two species within the South-east Asian Streak-eared Bulbul Pycnonotus blanfordi complex, in which both morphology and vocalizations have remained extremely similar. Despite a considerable pre-Pleistocene divergence of these two bulbul species, bioacoustic analysis failed to uncover differences in their main vocalization, but examination of live birds revealed important differences in eye color that had been overlooked in museum material. Our study demonstrates that genome-wide DNA data can be helpful in the detection of cryptic speciation, especially in species that have evolved limited morphological and behavioral differences.

Lautäußerungen der Sommergoldhähnchen von den Inseln Madeira und Mallorca (Regulus ignicapillus madeirensis, R. i. balearicus)@@@Vocalisations of Firecrests from the islands of Madeira and Mallorca (Regulus ignicapillus madeirensis, R. i. balearicus)

The vocal repertoire of two island populations of the Firecrest (R. ignicapillus) was studied. The song structure ofR. i. balearicus from Mallorca does not differ from that of nominateignicapillus, although intra- and interindividual variation of song types in Mallorca is higher than within continental populations, i.e. individual males use higher numbers of song types than nominateignicapillus in Central Europe. Several song types are terminated by distinct element groups strongly resembling song structures of North AfricanR. i. laeneni. The fixation of relatively rare element types and song patterns compared to Central EuropeanR. i. ignicapillus is explained by drift effects. The song repertoire of the individualR. i. madeirensis male is reduced to only one song type. This is divided into three phrases, two of them consisting of modified display and rage calls. While those song elements resemble innate calls, the reduction of learning opportunities which went along with the colonisation of Madeira is thought to be the main cause for the evolution of the Madeiran song type. Display calls are used in territorial contexts and differ greatly from those of other Firecrest subspecies in covering a larger frequency range and in including additional harmonics. Display calls are suspected to be a homologon of the excitement calls of nominateignicapillus, the “weija” note, which is also produced in subsong. Field experiments corroborate the evidence of a wide gap betweenR. i. madeirensis and nominateignicapillus song. Song and calls ofR. i. madeirensis do not evoke a notable territorial reaction in Central EuropeanR. i. ignicapillus, while the Madeiran Firecrests show strong reaction to the playback of Central and South-East European song types (ssp.ignicapillus andcaucasicus). Consequently,R. i. madeirensis is the only population of the Firecrest studied so far which differs considerably with respect to vocalisations from all four subspecies ofR. ignicapillus. Von den Inselpopulationen des Sommergoldhähnchens auf den Balearen (Mallorca),Regulus ignicapillus balearicus, und auf Madeira,R. i. madeirensis, wird die Struktur des Reviergesanges und der Rufe dargestellt. Ssp.madeirensis weicht in beiden markant von denen der Nominatform ab, ssp.balearicus nur im Strophenaufbau geringfügig. Die intra-und interindividuelle Variabilität der Strophentypen ist bei ssp.balearicus höher als auf dem Festland. Am Strophenende treten häufig Elementgruppen auf, die in Mitteleuropa fehlen. Seltene Elementtypen der Nominatform (ssp.ignicapillus) finden sich bei ssp.balearicus gehäuft, ähnlich wie bei ssp.laeneni (Nordafrika). Drift-Effekte gelten als Ursachen für die Unterschiede zwischen Balearen/N-Afrika und Mitteleuropa. Jedes ♂ von ssp.madeirensis benutzt nur einen Strophentyp; er variiert interindividuell stark. Die Strophe ist dreiphrasig und wird von modifizierten Kampf- und Erregungsrufen dominiert. Die Erregungsrufe sind stark frequenzmoduliert und weisen Obertöne auf, die in der Gesangsstrophe fehlen können. Wahrscheinlich sind die Erregungsrufe dem „Weia“-Element aus dem Subsong von ssp.ignicapillus homolog. Der hohe Anteil angeborener Rufe immadeirensis-Reviergesang wird mit Lernentzug der Erstsiedler begründet. Attrappenversuche belegen die markanten akustischen Differenzen zwischen Sommergoldhähnchen von Madeira und Mitteleuropa. Reviergesang und Erregungsrufe vonR. i. madeirensis werden von der Nominatform ssp.ignicapillus in Mitteleuropa nicht als artspezifisch erkannt. Die Madeira-Goldhähnchen reagieren hingegen auf mittel- und südosteuropäische Strophentypen (ssp.ignicapillus undcaucasicus) stark territorial.